The survival of organic matter in bone: a review
Open accessAbstract
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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A living tree growing at a German airport absorbed fossil fuel gases from passing planes and yielded a pMC of 28.8, or a 14C age of 10,000 14C years BP.
“In another case, a living tree growing at a German airport absorbed fossil fuel gases from passing planes.It yielded a pMC of 28.8, or a 14 C age of 10,000 14 C years BP [28].”
From The Search for Solutions to Mysterious Anomalies in the Geologic Column (2019) · cites this paper as [28]
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Greenlee, D. M. (1996) · ACS symposium series · doi:10.1021/bk-1996-0625.ch024 · Cited by 11 · see citing works
Towards an understanding of the decomposition of bone in the archaeological environment
Child, A. M. (1995) · Cited by 10 · see citing works
Montgelard, C. (1992) · Historical Biology · doi:10.1080/10292389209380437 · Cited by 9 · see citing works
Weser, U., Kaup, Y., Etspüler, H., Kenward, N., & Hedges, R. E. M. (1996) · Journal of Archaeological Science · doi:10.1006/jasc.1996.0068 · Cited by 9 · see citing works
Nitrogen and Fluorine Dating of Moundville Skeletal Samples
Haddy, A., & Hanson, A. K. (1982) · Cited by 6 · see citing works
Sonic velocity and the ultrastructure of mineralised tissues
Lees, S. (1989) · doi:10.1007/978-1-349-09868-2_6 · Cited by 6 · see citing works
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Strontium Isotopes from the Earth to the Archaeological Skeleton: A Review
Alexander Bentley, R. (2006) · Journal of Archaeological Method and Theory · doi:10.1007/s10816-006-9009-x · Cited by 1,311 · see citing works
“The pathways of diagenesis in bone, dentine and enamel, and in the organic and inorganic components of these tissues, vary markedly because of their chemical and structural differences, while the main external influences remain those of moisture and pH, microbial attack, temperature and time (Hare 1980; Collins et al.…”
BackgroundMethodLee‐Thorp, J. A. (2008) · Archaeometry · doi:10.1111/j.1475-4754.2008.00441.x · Cited by 747 · see citing works
Willerslev, E., & Cooper, A. (2005) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2004.2813 · Cited by 712 · see citing works
“It is important to note that negative blank controls may easily conceal low-level laboratory contamination owing to poorly understood carrier effects (Cooper 1993; Handt et al. 1994).”
BackgroundStable Isotope Analysis: A Tool for Studying Past Diet, Demography, and Life History
Katzenberg, M. A. (2007) · doi:10.1002/9780470245842.ch13 · Cited by 519 · see citing works
Optimal ancient DNA yields from the inner ear part of the human petrous bone
Pinhasi, R., Fernandes, D., Sirak, K., Novak, M., Connell, S., Alpaslan-Roodenberg, S., Gerritsen, F., Moiseyev, V., Gromov, A., Raczky, P., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129102 · Cited by 487 · see citing works
“While research has shown that the diagenetic status of the biomaterial from which aDNA will be extracted is correlated with the survival and preservation of DNA, the mechanisms of biomolecular deterioration as well as the location of DNA within the microscopic structure of the bone remain poorly understood [5].”
BackgroundIsotopic Study of the Biology of Modern and Fossil Vertebrates
Koch, P. L. (2007) · Wiley eBooks · doi:10.1002/9780470691854.ch5 · Cited by 437 · see citing works
Trueman, C. N., Behrensmeyer, A. K., Tuross, N., & Weiner, S. (2004) · Journal of Archaeological Science · doi:10.1016/j.jas.2003.11.003 · Cited by 426 · see citing works
Diagenesis of archaeological bone and tooth
Kendall, C., Eriksen, A., Kontopoulos, I., Collins, M. J., & Turner‐Walker, G. (2017) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2017.11.041 · Cited by 350 · see citing works
Self-citationBiomimetic remineralization of dentin
Niu, L., Zhang, W., Pashley, D. H., Breschi, L., Mao, J., Chen, J., & Tay, F. R. (2013) · Dental Materials · doi:10.1016/j.dental.2013.07.013 · Cited by 329 · see citing works
A guide to ancient protein studies
Hendy, J., Welker, F., Demarchi, B., Speller, C., Warinner, C., & Collins, M. J. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0510-x · Cited by 291 · see citing works
Self-citationFish bone chemistry and ultrastructure: implications for taphonomy and stable isotope analysis
Szpak, P. (2011) · Journal of Archaeological Science · doi:10.1016/j.jas.2011.07.022 · Cited by 284 · see citing works
“While still relatively understudied, these processes have received some attention within the context of mammalian bone (see Child, 1995; Collins et al., 2002).”
BackgroundImproving access to endogenous DNA in ancient bones and teeth
Damgaard, P. D. B., Margaryan, A., Schroeder, H., Orlando, L., Willerslev, E., & Allentoft, M. E. (2015) · Scientific Reports · doi:10.1038/srep11184 · Cited by 275 · see citing works
“Although the colonization of micro-organisms is likely heterogenous 26 , we expect that during the digestion of bone material in the first step of an aDNA extraction, surface contaminants will be released into solution first, regardless of their exact location of deposition.”
Reducing Microbial and Human Contamination in DNA Extractions from Ancient Bones and Teeth
Korlević, P., Gerber, T., Gansauge, M.-T., Hajdinjak, M., Nagel, S., Aximu‐Petri, A., & Meyer, M. (2015) · BioTechniques · doi:10.2144/000114320 · Cited by 267 · see citing works
“However, DNA preservation is highly variable and depends not only on the age of the material but also on environmental parameters at the excavation site (1,2).”
BackgroundThe thermal history of human fossils and the likelihood of successful DNA amplification
Smith, C. I., Chamberlain, A. T., Riley, M. S., Stringer, C. B., & Collins, M. J. (2003) · Journal of Human Evolution · doi:10.1016/s0047-2484(03)00106-4 · Cited by 270 · see citing works
Self-citationTsutaya, T., & Yoneda, M. (2014) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22657 · Cited by 252 · see citing works
Survival and recovery of DNA from ancient teeth and bones
Adler, C. J., Haak, W., Donlon, D., & Cooper, A. (2010) · Journal of Archaeological Science · doi:10.1016/j.jas.2010.11.010 · Cited by 217 · see citing works
“As a result, the differences in DNA degradation between samples are commonly attributed to environmental factors (Alvarez Garcia et al., 1996; Collins et al., 2002; Dobberstein et al., 2008), especially temperature (Smith et al.”
BackgroundResultBone diagenesis in the European Holocene I: patterns and mechanisms
Smith, C. I., Nielsen-Marsh, C. M., Jans, M. M. E., & Collins, M. J. (2007) · Journal of Archaeological Science · doi:10.1016/j.jas.2006.11.006 · Cited by 217 · see citing works
Self-citationDecomposition of Human Remains
Janaway, R. C., Percival, S. L., & Wilson, A. S. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-327-1_14 · Cited by 216 · see citing works
Bone diagenesis in the European Holocene II: taphonomic and environmental considerations
Nielsen-Marsh, C. M., Smith, C. I., Jans, M. M. E., Nord, A. G., Kars, H., & Collins, M. J. (2007) · Journal of Archaeological Science · doi:10.1016/j.jas.2006.11.012 · Cited by 210 · see citing works
Self-citationWhy do crystallinity values fail to predict the extent of diagenetic alteration of bone mineral?
Trueman, C. N., Privat, K. L., & Field, J. H. (2008) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2008.03.038 · Cited by 203 · see citing works
The Bioarchaeology of Children
Lewis, M. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542473 · Cited by 199 · see citing works
Lebon, M., Reiche, I., Bahain, J., Chadefaux, C., Moigne, A., Fröhlich, F., Sémah, F., Schwarcz, H., & Falguères, C. (2010) · Journal of Archaeological Science · doi:10.1016/j.jas.2010.03.024 · Cited by 176 · see citing works
“…crystallinity, to be discussed below, a parameter re fl ecting the degree of perfection of the lattice, and the crystal size, as a result of dissolution/recrystallization processes (Collins et al., 2002; Hedges, 2002; Hedges and Millard, 1995; Reiche et al., 1999, 2003; Trueman et al., 2008).”
BackgroundMethodDNA in ancient bone – Where is it located and how should we extract it?
Campos, P. F., Craig, O. E., Turner‐Walker, G., Peacock, E. E., Willerslev, E., & Gilbert, M. T. P. (2011) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2011.07.003 · Cited by 181 · see citing works
Self-citationProteins in Art, Archaeology, and Paleontology: From Detection to Identification
Dallongeville, S., Garnier, N., Rolando, C. H., & Tokarski, C. (2015) · Chemical Reviews · doi:10.1021/acs.chemrev.5b00037 · Cited by 170 · see citing works
Schwarz, C., Debruyne, R., Kuch, M., McNally, E. A., Schwarcz, H. P., Aubrey, A. D., Bada, J. L., & Poinar, H. N. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp159 · Cited by 168 · see citing works
“Bone is a composite tissue comprised of both organic (mainly collagen) and inorganic matter (bioapatite) (32).”
BackgroundGuiry, E. J., & Szpak, P. (2021) · Journal of Archaeological Science · doi:10.1016/j.jas.2021.105416 · Cited by 165 · see citing works
Bone preservation and DNA amplification
Götherström, A., Collins, M. J., Angerbjörn, A., & Lidén, K. (2002) · Archaeometry · doi:10.1111/1475-4754.00072 · Cited by 164 · see citing works
Self-citationMunro, L. E., Longstaffe, F. J., & White, C. D. (2007) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2007.01.011 · Cited by 163 · see citing works
“The structure and chemical composition of bone can be altered after death by natural processes such as weathering, dissolution, precipitation, microbial remodeling, mineral replacement, ionic substitution, recrystallization and isotopic exchange (Pate and Hutton, 1988; Collins et al., 2002; Hedges, 2002; Lee-Thorp, 20…”
BackgroundEthanol Wet-bonding Challenges Current Anti-degradation Strategy
Sadek, F. T., Braga, R. R., Muench, A., Liu, Y., Pashley, D. H., & Tay, F. R. (2010) · Journal of Dental Research · doi:10.1177/0022034510385240 · Cited by 162 · see citing works
“Conversely, removal of intrafibrillar water via apatite replacement conserves the integrity of the collagen matrix in mineralized tissues over a much longer time span (Collins et al., 2002) than is possible with hydrophilic dentin adhesives.”
BackgroundSuccess rates of nuclear short tandem repeat typing from different skeletal elements.
Milos, A., Selmanović, A., Smajlović-Skenderagić, L., Huel, R., Katzmarzyk, C., Rizvić, A., & Parsons, T. J. (2007) · PubMed Central · Cited by 161 · see citing works
Brock, F., Higham, T., & Ramsey, C. B. (2009) · Journal of Archaeological Science · doi:10.1016/j.jas.2009.11.015 · Cited by 158 · see citing works
Gonçalves, D., Thompson, T. J. U., & Cunha, E. M. (2011) · Journal of Archaeological Science · doi:10.1016/j.jas.2011.01.006 · Cited by 153 · see citing works
DNA recovery and analysis from skeletal material in modern forensic contexts
Latham, K. E., & Miller, J. J. (2018) · Forensic Sciences Research · doi:10.1080/20961790.2018.1515594 · Cited by 153 · see citing works
The taphonomy of cooked bone: characterizing boiling and its physico–chemical effects
Roberts, S. J., Smith, C. I., Millard, A. R., & Collins, M. J. (2002) · Archaeometry · doi:10.1111/1475-4754.t01-1-00080 · Cited by 151 · see citing works
“That the traces for deproteinated bone and severely boiled bone are similar is to be expected, as collagen is lost through chemically mediated hydrolysis (Collins et al. 1995) in both cases, accelerated by different mechanisms (hydrazine hydrate and increased temperature).”
BackgroundSelf-citationAncient protein analysis in archaeology
Hendy, J. (2021) · Science Advances · doi:10.1126/sciadv.abb9314 · Cited by 148 · see citing works
Single amino acid radiocarbon dating of Upper Paleolithic modern humans
Marom, A., McCullagh, J., Higham, T., Sinitsyn, A. A., & Hedges, R. E. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1116328109 · Cited by 138 · see citing works
“However, the extracted bulk gelatin can be heterogeneous and include, or be cross-linked to, potential contaminants from the depositional environment, such as humic and fulvic acids, rootlets, cellulose, sediments, and other plant and animal remains including amino acids from bacteria and microorganisms (1, 2).”
BackgroundRapid Quantification of Bone Collagen Content by ATR-FTIR Spectroscopy
Lebon, M., Reiche, I., Gallet, X., Bellot‐Gurlet, L., & Zazzo, A. (2016) · Radiocarbon · doi:10.1017/rdc.2015.11 · Cited by 137 · see citing works
“…(3) Then, considering that a modern bone contain around 22wt% of collagen and consequently 4wt% of nitrogen (Stafford et al. 1988; van Klinken 1999; Collins et al. 2002), the wt% of collagen remaining in archaeological bone can be calculated by ATR-FTIR using Equation 4 with a standard error of…”
MethodFrom bone to fossil: A review of the diagenesis of bioapatite
Keenan, S. W. (2016) · American Mineralogist · doi:10.2138/am-2016-5737 · Cited by 134 · see citing works
Soft Tissue Preservation in Terrestrial Mesozoic Vertebrates
Schweitzer, M. H. (2011) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-040610-133502 · Cited by 133 · see citing works
Tütken, T., Vennemann, T. W., & Pfretzschner, H. (2008) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2008.03.037 · Cited by 131 · see citing works
“This is to be expected because biogenic apatite and collagen are tightly cross-linked, so their fates are strongly dependent on the hydrolytic and/or bacterial collagen degradation, implying that apatite and collagen diagenesis should proceed simultaneously (e.g. Tuross et al., 1989; Hedges et al., 1995; Collins et al…”
Primum non nocere – The effects of sodium hypochlorite on dentin as used in endodontics
Gu, L.-S., Huang, X.-Q., Griffin, B., Bergeron, B. E., Pashley, D. H., Niu, L., & Tay, F. R. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.08.008 · Cited by 128 · see citing works
Schweitzer, M. H., Wittmeyer, J. L., & Horner, J. R. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3705 · Cited by 123 · see citing works
Bertrand, L., Bernard, S., Marone, F., Thoury, M., Reiche, I., Gourrier, A., Sciau, P., & Bergmann, U. (2016) · Topics in Current Chemistry · doi:10.1007/s41061-015-0003-1 · Cited by 120 · see citing works
The critical barrier to progress in dentine bonding with the etch-and-rinse technique
Brackett, M. G., Li, N., Brackett, W. W., Sword, R. J., Qi, Y.-P., Niu, L., Pucci, C. R., Dib, A., Pashley, D. H., & Tay, F. R. (2011) · Journal of Dentistry · doi:10.1016/j.jdent.2010.12.009 · Cited by 117 · see citing works
Carbodiimide Cross-linking Inactivates Soluble and Matrix-bound MMPs, in vitro
Tezvergil‐Mutluay, A., Mutluay, M. M., Agee, K. A., SESEOGULLARI-DIRIHAN, R., Hoshika, T., Cadenaro, M., Breschi, L., VALLITTU, P. K., Tay, F. R., & Pashley, D. H. (2011) · Journal of Dental Research · doi:10.1177/0022034511427705 · Cited by 111 · see citing works
“Acid-etching of dentin exposes matrix metalloproteinases (MMPs) which are inactive in mineralized dentin and bone (Collins et al., 2002; Breschi et al., 2010).”
BackgroundCherkinsky, A. (2009) · Radiocarbon · doi:10.1017/s0033822200055995 · Cited by 117 · see citing works
“Recent publications show that such problems still exist and suggest that they are caused by both the poor preservation of collagen and the difficulties in removing contaminants from the bone extracts used for dating (Koch et al. 1997; Collins et al. 2002; Ambrose and Krigbaum 2003).”
BackgroundPrinciples of demineralization: Modern strategies for the isolation of organic frameworks
Ehrlich, H., Koutsoukos, P. G., Demadis, K. D., & Сергеевич, П. О. (2008) · Micron · doi:10.1016/j.micron.2008.02.004 · Cited by 109 · see citing works
“…matrix (protein, polysaccharide, lipid) and mineral, then three pathways of demineralization in the natural environment have been identified (Collins et al., 2002): c hemical deterioration of the organic phase (1); c hemical deterioration of the mineral phase (2); b iological…”
BackgroundInfluentialProducts and Applications of Biopolymers
Verbeek, C. J. R. (2012) · InTech eBooks · doi:10.5772/1802 · Cited by 109 · see citing works
Takano, Y., Kashiyama, Y., Ogawa, N. O., Chikaraishi, Y., & Ohkouchi, N. (2010) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.4651 · Cited by 108 · see citing works
Roberts, P., Fernandes, R., Craig, O. E., Larsen, T., Lucquin, A., Swift, J., & Zech, J. (2017) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.8044 · Cited by 102 · see citing works
“Furthermore, the mechanisms behind these changes, especially for tooth enamel bioapatite and bone collagen, are relatively well known.(5,18,21) While this has led to basic diagenetic checks that are applied in many archaeological science publications (Table 1), this information often goes unpublished or is not utilized”
Carbon Nanotubes and Graphene as Nanoreinforcements in Metallic Biomaterials: a Review
Munir, K. S., Wen, C., & Li, Y. (2019) · Advanced Biosystems · doi:10.1002/adbi.201800212 · Cited by 102 · see citing works
Schroeter, E. R., DeHart, C. J., Cleland, T. P., Zheng, W., Thomas, P. M., Kelleher, N. L., Bern, M. W., & Schweitzer, M. H. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00873 · Cited by 99 · see citing works
Early diagenesis and recrystallization of bone
Keenan, S. W., & Engel, A. S. (2016) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2016.09.033 · Cited by 96 · see citing works
Kim, Y. K., Mai, S., Mazzoni, A., Liu, Y., Tezvergil‐Mutluay, A., Takahashi, K., Zhang, K., Pashley, D. H., & Tay, F. R. (2010) · Acta Biomaterialia · doi:10.1016/j.actbio.2010.03.021 · Cited by 97 · see citing works
“Moreover, these host-derived, collagen-bound enzymes [36] may be fossilized by the intrafibrillar crystallites that are deposited within and on the collagen fibrils [20].”
BackgroundQuality control for modern bone collagen stable carbon and nitrogen isotope measurements
Guiry, E. J., & Szpak, P. (2020) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.13433 · Cited by 94 · see citing works
“…acids from the burial environment) carbon sources or collagen deterioration (selective amino acid loss) resulting in a disproportionate loss of either carbon or nitrogen (for reviews, see Collins & Galley, 1998; Collins et al., 2002; Collins, Riley, Child, & Turner-Walker, 1995; Van Klinken, 1999).”
BackgroundHarbeck, M., & Grupe, G. (2009) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-009-0004-5 · Cited by 92 · see citing works
“It should however be considered that degradation processes during the inhumation period can lead to structural alterations in the bone tissue or even a total loss of molecules (e.g. Collins et al. 2002; Hedges 2002).”
BackgroundEffects of Calcium Silicate–based Materials on Collagen Matrix Integrity of Mineralized Dentin
Leiendecker, A. P., Qi, Y., Sawyer, A. N., Niu, L., Agee, K. A., Loushine, R. J., Weller, R. N., Pashley, D. H., & Tay, F. R. (2012) · Journal of Endodontics · doi:10.1016/j.joen.2012.01.004 · Cited by 92 · see citing works
Analysis of Bone “Collagen” Extraction Products for Radiocarbon Dating
Brock, F., Geoghegan, V., Thomas, B., Jurkschat, K., & Higham, T. (2013) · Radiocarbon · doi:10.1017/s0033822200057581 · Cited by 88 · see citing works
“The processes involved in bone diagenesis are complex and still poorly understood (e.g. Hedges and Law 1989; Collins et al. 1995, 2002).”
BackgroundTaphonomy and the Nature of Archaeological Assemblages
Stodder, A. L. W. (2007) · doi:10.1002/9780470245842.ch3 · Cited by 87 · see citing works
Proteome degradation in ancient bone: Diagenesis and phylogenetic potential
Buckley, M., & Wadsworth, C. (2014) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2014.06.026 · Cited by 84 · see citing works
Trueman, C. N., Palmer, M. R., Field, J. H., Privat, K. L., Ludgate, N., Chavagnac, V., Eberth, D. A., Cifelli, R. L., & Rogers, R. R. (2008) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2008.02.006 · Cited by 82 · see citing works
“Collagen fills ca. 25 –36% of the volume of bone material in vivo [7,12], so in a fully recrystallised bone at least 25% of the volume must be composed of calcium phosphate that is entirely exogenous to the original bone ions.”
BackgroundKjellström, A., Storå, J., Possnert, G., & Linderholm, A. E. (2009) · Journal of Archaeological Science · doi:10.1016/j.jas.2009.08.007 · Cited by 83 · see citing works
“In addition, several parameters are involved in the loss of collagen from bone, the main ones being time, temperature and pH (Collins et al., 2002; Hedges, 2002).”
Hill, R. C., Wither, M. J., Nemkov, T. G., Barrett, A. S., D’Alessandro, A., Dzieciątkowska, M., & Hansen, K. C. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.047787 · Cited by 81 · see citing works
“The second most abundant bone protein (2, 6, 65) osteocalcin (BGLAP), was identified here by all of the software packages used for searching (Table I).”
BackgroundMethodInfluentialHigh‐Throughput DNA sequencing of ancient wood
Wagner, S., Lagane, F., Seguin‐Orlando, A., Schubert, M., Leroy, T., Guichoux, E., Chancerel, É., Bech-Hebelstrup, I., Bernard, V., Billard, C., et al. (2018) · Molecular Ecology · doi:10.1111/mec.14514 · Cited by 79 · see citing works
“Only two taphonomical contexts, corresponding to aerobic and/or acidic environments known to accelerate DNA decay (Collins et al. 2002; Smith et al. 2003; Nielsen-Marsh et al. 2007), were not amenable to DNA sequencing.”
BackgroundParker, G. J., McKiernan, H. E., Legg, K. M., & Goecker, Z. C. (2021) · Forensic Science International Genetics · doi:10.1016/j.fsigen.2021.102529 · Cited by 78 · see citing works
Katzenberg, M. A., & Waters‐Rist, A. L. (2018) · doi:10.1002/9781119151647.ch14 · Cited by 78 · see citing works
Bone collagen preservation in the tropics: a case study from ancient Puerto Rico
Pestle, W. J., & Colvard, M. D. (2012) · Journal of Archaeological Science · doi:10.1016/j.jas.2012.03.008 · Cited by 77 · see citing works
Preparation of bone powder for FTIR-ATR analysis: The particle size effect
Kontopoulos, I., Presslee, S., Penkman, K., & Collins, M. (2018) · Vibrational Spectroscopy · doi:10.1016/j.vibspec.2018.09.004 · Cited by 78 · see citing works
Self-citationPahlavani, H., Amani, M., Saldívar, M. C., Zhou, J., Mirzaali, M. J., & ZADPOOR, A. A. (2022) · Communications Materials · doi:10.1038/s43246-022-00270-2 · Cited by 77 · see citing works
“Many other design features found in nature, such as hierarchical micro-architectures [10], [11], [12], [13], functional gradients (in terms of both geometries and material properties) [14], [15], and softhard composites (similar to the organic and mineral phases in bone [11], [16], [17]) can be also realized to expand…”
BackgroundDiagenesis and survival of osteocalcin in archaeological bone
Smith, C. I., Craig, O. E., Prigodich, R. V., Nielsen-Marsh, C. M., Jans, M. M. E., Vermeer, C., & Collins, M. J. (2004) · Journal of Archaeological Science · doi:10.1016/j.jas.2004.07.003 · Cited by 76 · see citing works
“The diagenesis of organic matter in archaeological bone is a complex phenomenon [10].”
BackgroundSelf-citationSasso, G. D., Lebon, M., Angelini, I., Maritan, L., Usai, D., & Artioli, G. (2016) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2016.10.005 · Cited by 70 · see citing works
Fossil bones and teeth: Preservation or alteration of biogenic compositions?
Tütken, T., & Vennemann, T. W. (2011) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2011.06.020 · Cited by 74 · see citing works
“…usually only preserved in Holocene or Late Pleistocene skeletal remains (e.g., Hagelberg et al., 1994; Greenwood et al., 1999; Jones et al., 2001; Collins et al., 2002; Adler et al., 2011; Bocherens et al., 2011) and only rarely reported for pre-Quaternary specimens (e.g., Asara et al., 2007;…”
BackgroundKlein, N., Scheyer, T. M., & Tütken, T. (2009) · Fossil record · doi:10.1002/mmng.200900002 · Cited by 73 · see citing works
“Nitrogen is exclusively found in the protein phase of bone (predominantly collagen) (Francillon-Vieillot et al. 1990; Collins et al. 2002).”
BackgroundNalawade-Chavan, S., McCullagh, J., & Hedges, R. E. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0076896 · Cited by 72 · see citing works
“Crossed-linked contaminants are difficult to remove using routine methods [9], [10].”
Novel Substrates as Sources of Ancient DNA: Prospects and Hurdles
Green, E. J., & Speller, C. (2017) · Genes · doi:10.3390/genes8070180 · Cited by 67 · see citing works
López‐Costas, O., Suárez, Ó. L., & Cortizas, A. M. (2016) · Journal of Archaeological Science · doi:10.1016/j.jas.2016.02.001 · Cited by 69 · see citing works
Collagen Fingerprinting: A New Screening Technique for Radiocarbon Dating Ancient Bone
Harvey, V. L., Egerton, V. M., Chamberlain, A. T., Manning, P. L., & Buckley, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150650 · Cited by 69 · see citing works
“Surprisingly little work has been conducted on bone collagen preservation in the tropics, although it is well known that collagen survival is subject to a number of factors that work synergistically to facilitate degradation; namely time, temperature, bacterial presence, geochemistry and hydrology [32, 33].”
BackgroundScreening archaeological bone for palaeogenetic and palaeoproteomic studies
Kontopoulos, I., Penkman, K. E. H., Mullin, V. E., Winkelbach, L., Unterländer, M., Scheu, A., Kreutzer, S., Hansen, H. B., Margaryan, A., Teasdale, M. D., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0235146 · Cited by 68 · see citing works
“Although proteins are more stable than DNA, and can therefore survive much longer (e.g. [32] and references therein), the dominant protein in bone (collagen) also suffers post-mortem from biological, chemical, and environmental factors [33–35].”
BackgroundSelf-citationBritton, K., Gaudzinski‐Windheuser, S., Roebroeks, W., Kindler, L., & Richards, M. P. (2012) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2012.03.028 · Cited by 69 · see citing works
“Collagen molecules break-down through time in the burial environment, and the processes of diagenesis, hydrolysis and microbial attack can serve to degrade collagen, resulting in its loss or in the alteration of in vivo stable isotope signatures (Ambrose, 1990; van Klinken, 1999; Collins et al., 2002; Nielsen-Marsh et…”
BackgroundHuman auditory ossicles as an alternative optimal source of ancient DNAPreprint
Sirak, K. A., Fernandes, D., Cheronet, O., Harney, É., Mah, M., Mallick, S., Rohland, N., Adamski, N., Broomandkhoshbacht, N., Callan, K. A., et al. (2020) · Genome Research · doi:10.1101/gr.260141.119 · Cited by 69 · see citing works
The temporal degradation of bone collagen: A histochemical approach
Boaks, A., Siwek, D. F., & Mortazavi, F. (2014) · Forensic Science International · doi:10.1016/j.forsciint.2014.04.008 · Cited by 68 · see citing works
Estimation of the pre-burning condition of human remains in forensic contexts
Gonçalves, D., Cunha, E. M., & Thompson, T. J. U. (2014) · International Journal of Legal Medicine · doi:10.1007/s00414-014-1027-8 · Cited by 66 · see citing works
Petrous bone diagenesis: a multi-analytical approach
Kontopoulos, I., Penkman, K. E. H., McAllister, G. D., Lynnerup, N., Damgaard, P. D. B., Hansen, H. B., Allentoft, M. E., & Collins, M. J. (2019) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2019.01.005 · Cited by 68 · see citing works
Self-citationExperimental taphonomy: post-mortem microstructural modifications in Sus scrofa domesticus bone
Kontopoulos, I., Nystrom, P., & White, L. (2016) · Forensic Science International · doi:10.1016/j.forsciint.2016.06.024 · Cited by 67 · see citing works
Mickleburgh, H. L., Schwalbe, E. C., Bonicelli, A., Mizukami, H., Sellitto, F., Starace, S., Wescott, D. J., Carter, D. O., & Procopio, N. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00992 · Cited by 65 · see citing works
Müller, K., Chadefaux, C., Thomas, N., & Reiche, I. (2011) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2011.03.023 · Cited by 65 · see citing works
Webb, E. C., White, C. D., & Longstaffe, F. J. (2014) · Journal of Archaeological Science · doi:10.1016/j.jas.2014.07.001 · Cited by 63 · see citing works
“Sample loss is expected for bone, since pre-treatment involves removal of organic material (~22% by weight in fresh bone, but less in archaeological bone; Hedges and Law, 1989; Collins et al., 2002).”
BackgroundEmpirical evaluation of bone extraction protocols
Cleland, T. P., Voegele, K., & Schweitzer, M. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031443 · Cited by 60 · see citing works
“, [55,56, 57,58]) because they are the two most abundant proteins in extant bone and both have high potential for preservation [6].”
BackgroundMicrospectroscopic evidence of cretaceous bone proteins
Lindgren, J., Uvdal, P., Engdahl, A., Lee, A. H., Alwmark, C., Bergquist, K.-E., Nilsson, E., Ekström, P., Rasmussen, M., Douglas, D. A., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019445 · Cited by 61 · see citing works
“bone (Figure 1M) [33], which in IRSNB 1624 may have been”
Grunenwald, A., Keyser, C., Sautereau, A., Crubézy, É., Ludes, B., & Drouet, C. (2013) · Applied Surface Science · doi:10.1016/j.apsusc.2013.12.063 · Cited by 60 · see citing works
Dinosaur Peptides Suggest Mechanisms of Protein Survival
Antonio, J. D. S., Schweitzer, M. H., Jensen, S. T., Kalluri, R., Buckley, M., & Orgel, J. P. R. O. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020381 · Cited by 58 · see citing works
“[18,26,27,28,29,30]).”
Barrett, J. H. (2019) · Journal of Fish Biology · doi:10.1111/jfb.13929 · Cited by 57 · see citing works
Díaz-Maroto, P. F., Rey‐Iglesia, A., Cartajena, I., Lautaro Núñez, A., Westbury, M. V., Varas, V., Moraga, M. L., Campos, P. F., Orozco‐terWengel, P., Marín, J. C., et al. (2021) · eLife · doi:10.7554/elife.63390 · Cited by 56 · see citing works
Speller, C., van den Hurk, Y., Charpentier, A., Rodrigues, A. S. L., Gardeisen, A., Wilkens, B., McGrath, K. M., Rowsell, K., Spindler, L., Collins, M. J., et al. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0332 · Cited by 57 · see citing works
Self-citationMüller, K., & Reiche, I. (2011) · Journal of Archaeological Science · doi:10.1016/j.jas.2011.06.029 · Cited by 56 · see citing works
“Numerous researches have been carried out aiming at a better understanding of the diagenetic and taphonomic alteration of bone during burial time depending on the respective environmental conditions (e.g. Weiner and Bar-Yosef, 1990; Hedges et al., 1995; Reiche et al., 1999, 2001, 2003; Collins et al., 2002; Trueman et…”
BackgroundBone and Other Skeletal Tissues
Villagrán, X. S., Huisman, D. J., Mentzer, S. M., Miller, C. E., & Jans, M. M. E. (2017) · doi:10.1002/9781118941065.ch1 · Cited by 56 · see citing works
Niu, L., Jiao, K., Qi, Y., Nikonov, S. Y., Yiu, C. K. Y., Arola, D. D., Gong, S., Elmarakby, A. A., Carrilho, M., Hamrick, M. W., et al. (2012) · The FASEB Journal · doi:10.1096/fj.12-210211 · Cited by 55 · see citing works
Association between ancient bone preservation and dna yield: A multidisciplinary approach
Sosa, C., Vispe, E., Núńez, C., Baeta, M., Casalod, Y., Bolea, M., Hedges, R. E. M., & Martínez‐Jarreta, B. (2013) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22262 · Cited by 54 · see citing works
Grieshaber, B. M., Osborne, D. L., Doubleday, A. F., & Kaestle, F. A. (2007) · Journal of Archaeological Science · doi:10.1016/j.jas.2007.06.001 · Cited by 54 · see citing works
“…concern was paramount, as previous research and the authors’ personal experience suggest that small differences in depositional characteristics can have major effects on the preservation of DNA, even within remains recovered from a single site (e.g., Burger et al., 1999; Collins et al., 2002).”
Talamo, S., Fewlass, H., Maria, R., & Jaouen, K. (2021) · STAR Science & Technology of Archaeological Research · doi:10.1080/20548923.2021.1944479 · Cited by 54 · see citing works
“The molecule is comprised of three peptide chains organised in a triple helix structure with a molecular weight of ∼ 285-300 kDa ( ∼ 90-100 kDa for each a peptide chain) (Furthmayr and Timpl 1971; Collins et al. 2002; Zhang, Li, and Shi 2006; Garnero 2015).”
Influential
- 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)
- Venue
- Archaeometry
- Publisher
- Wiley
- Published
- 2002-08
- Volume
- 44
- Issue
- 3
- Pages
- 383-394
- ISSN
- 0003-813X (ISSN-L)
- 1475-4754
- 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
- 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
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Archaeology and ancient environmental studies
- Social Sciences › Arts and Humanities › Archeology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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