A fresh perspective on infrared spectroscopy as a prescreening method for molecular and stable isotopes analyses on ancient human bones.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
10 Jan 2024
10 Jan 2024
Historique:
received:
08
06
2023
accepted:
06
01
2024
medline:
11
1
2024
pubmed:
11
1
2024
entrez:
10
1
2024
Statut:
epublish
Résumé
Following the development of modern genome sequencing technologies, the investigation of museum osteological finds is increasingly informative and popular. Viable protocols to help preserve these collections from exceedingly invasive analyses, would allow greater access to the specimens for scientific research. The main aim of this work is to survey skeletal tissues, specifically petrous bones and roots of teeth, using infrared spectroscopy as a prescreening method to assess the bone quality for molecular analyses. This approach could overcome the major problem of identifying useful genetic material in archaeological bone collections without resorting to demanding, time consuming and expensive laboratory studies. A minimally invasive sampling of archaeological bones was developed and bone structural and compositional changes were examined, linking isotopic and genetic data to infrared spectra. The predictive model based on Infrared parameters is effective in determining the occurrence of ancient DNA (aDNA); however, the quality/quantity of aDNA cannot be determined because of the influence of environmental and local factors experienced by the examined bones during the burial period.
Identifiants
pubmed: 38200208
doi: 10.1038/s41598-024-51518-5
pii: 10.1038/s41598-024-51518-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1028Subventions
Organisme : Fondazione Cassa di Risparmio di Padova e Rovigo
ID : Ph.D. scholarship
Organisme : Consorzio Interuniversitario Nazionale per la Scienza e Tecnologia dei Materiali
ID : scholarship
Informations de copyright
© 2024. The Author(s).
Références
Parker, C. et al. A systematic investigation of human DNA preservation in medieval skeletons. Sci. Rep. 10, 18225 (2020).
pubmed: 33106554
pmcid: 7588426
doi: 10.1038/s41598-020-75163-w
Hansen, H. B. et al. Comparing ancient DNA preservation in petrous bone and tooth cementum. PLoS One 12, 1–18 (2017).
doi: 10.1371/journal.pone.0170940
Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).
pubmed: 25334030
doi: 10.1038/ncomms6257
Fratzl, P., Gupta, H. S., Paschalis, E. P. & Roschger, P. Structure and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 14, 2115–2123 (2004).
doi: 10.1039/B402005G
Reznikov, N., Bilton, M., Lari, L., Stevens, M. M. & Kröger, R. Fractal-like hierarchical organization of bone begins at the nanoscale. Science 360, 6388 (2018).
doi: 10.1126/science.aao2189
Dey, P. Bone mineralisation. Intech 32, 137–144 (2020).
Shoulders, M. D. & Raines, R. T. Collagen structure and stability. Annu. Rev. Biochem. 78, 929–958 (2009).
pubmed: 19344236
pmcid: 2846778
doi: 10.1146/annurev.biochem.77.032207.120833
Florencio-Silva, R., da Sasso, G. R., Sasso-Cerri, E., Simões, M. J. & Cerri, P. S. Biology of bone tissue: Structure, function, and factors that influence bone cells. Biomed Res. Int. 2015, 1–17 (2015).
doi: 10.1155/2015/421746
Chen, H. & Liu, Y. Teeth. In Advanced Ceramics for Dentistry 5–21 (Elsevier, 2014). https://doi.org/10.1016/B978-0-12-394619-5.00002-X .
doi: 10.1016/B978-0-12-394619-5.00002-X
Trammell, L. & Kroman, A. M. Bone and Dental Histology. In Research Methods in Human Skeletal Biology (eds DiGangi, E. A. & Moore, M. K.) (Elsevier, 2013).
Trueman, C. N. et al. Comparing rates of recrystallisation and the potential for preservation of biomolecules from the distribution of trace elements in fossil bones. Comptes Rendus - Palevol 7, 145–158 (2008).
doi: 10.1016/j.crpv.2008.02.006
Collins, M. J. et al. The survival of organic matter in bone: A review. Archaeometry 44, 383–394 (2002).
doi: 10.1111/1475-4754.t01-1-00071
Collins, M. J., Riley, M. S., Child, A. M. & Turner-Walker, G. A basic mathematical simulation of the chemical degradation of ancient collagen. J. Archaeol. Sci. 22, 175–183 (1995).
doi: 10.1006/jasc.1995.0019
Rudakova, T. E. & Zaikov, G. E. Degradation of collagen and its possible applications in medicine. Polym. Degrad. Stab. 18, 271–291 (1987).
doi: 10.1016/0141-3910(87)90015-2
Berna, F., Matthews, A. & Weiner, S. Solubilities of bone mineral from archaeological sites: The recrystallization window. J. Archaeol. Sci. 31, 867–882 (2004).
doi: 10.1016/j.jas.2003.12.003
Hedges, R. E. M. Bone diagenesis: An overview of processes. Archaeometry 44, 319–328 (2002).
doi: 10.1111/1475-4754.00064
Klont, B., Damen, J. J. M. & ten Cate, J. M. Degradation of bovine incisor root collagen in an in vitro caries model. Arch. Oral Biol. 36, 299–304 (1991).
pubmed: 1648345
doi: 10.1016/0003-9969(91)90100-9
Nielsen-Marsh, C. M. & Hedges, R. E. M. Patterns of diagenesis in bone I: The effects of site environments. J. Archaeol. Sci. 27, 1139–1150 (2000).
doi: 10.1006/jasc.1999.0537
Reiche, I. et al. A multi-analytical study of bone diagenesis: The Neolithic site of Bercy (Paris, France). Meas. Sci. Technol. 14, 1608–1619 (2003).
doi: 10.1088/0957-0233/14/9/312
Trueman, C. N. G., Behrensmeyer, A. K., Tuross, N. & Weiner, S. Mineralogical and compositional changes in bones exposed on soil surfaces in Amboseli National Park, Kenya: Diagenetic mechanisms and the role of sediment pore fluids. J. Archaeol. Sci. 31, 721–739 (2004).
doi: 10.1016/j.jas.2003.11.003
Hedges, R. E. M. & Millard, A. R. Bones and groundwater: Towards the modelling of diagenetic processes. J. Archaeol. Sci. 22, 155–164 (1995).
doi: 10.1006/jasc.1995.0017
Allentoft, M. E. et al. The half-life of DNA in bone: Measuring decay kinetics in 158 dated fossils. Proc. R. Soc. B Biol. Sci. 279, 4724–4733 (2012).
doi: 10.1098/rspb.2012.1745
Rollo, F., Ubaldi, M., Marota, I., Luciani, S. & Ermini, L. DNA Diagenesis: Effect of environment and time on human bone. Anc. Biomol. 4, 1–7 (2002).
Damgaard, P. B. et al. Improving access to endogenous DNA in ancient bones and teeth. Sci. Rep. 5, 1–12 (2015).
doi: 10.1038/srep11184
Carpenter, M. L. et al. Pulling out the 1%: Whole-Genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 93, 852–864 (2013).
pubmed: 24568772
pmcid: 3824117
doi: 10.1016/j.ajhg.2013.10.002
Der Sarkissian, C. et al. Ancient genomics. Philos. Trans. R. Soc. B Biol. Sci. 370, 1660 (2015).
Campos, P. F. et al. DNA in ancient bone - Where is it located and how should we extract it?. Ann. Anat. 194, 7–16 (2012).
pubmed: 21855309
doi: 10.1016/j.aanat.2011.07.003
Sosa, C. et al. Association between ancient bone preservation and DNA yield: A multidisciplinary approach. Am. J. Phys. Anthropol. 151, 102–109 (2013).
pubmed: 23595645
doi: 10.1002/ajpa.22262
Rohland, N. & Hofreiter, M. Comparison and optimization of ancient DNA extraction. Biotechniques 42, 343–352 (2007).
pubmed: 17390541
doi: 10.2144/000112383
Aneli, S. et al. The genetic origin of daunians and the pan-mediterranean southern Italian iron age context. Mol. Biol. Evol. 39, 1–16 (2022).
doi: 10.1093/molbev/msac014
Saupe, T. et al. Ancient genomes reveal structural shifts after the arrival of Steppe-related ancestry in the Italian Peninsula. Curr. Biol. 31, 2576-2591.e12 (2021).
pubmed: 33974848
doi: 10.1016/j.cub.2021.04.022
Mays, S., Edlers, J., Humphrey, L., White, W. & Marshall, P. Science and the Dead: A Guideline for the Destructive Sampling of Archaeological Human Remains for Scientific Analysis. (2013).
Orlando, L. et al. Ancient DNA analysis. Nat. Rev. Methods Primers https://doi.org/10.1038/s43586-020-00011-0 (2021).
doi: 10.1038/s43586-020-00011-0
Balzeau, A. Comparative aspects of temporal bone pneumatization in some African fossil hominins. BMSAP 27, 135–141 (2015).
doi: 10.1007/s13219-015-0126-5
Brace, C. L., Smith, S. L. & Hunt, K. D. What big teeth you had, Grandma! Human tooth size, past and present. In Advances in Dental Anthropology (eds Kelley, M. K. & Larsen, C. S.) 33–57 (Wiley-Liss, 1991).
Demes, B. & Creel, N. Bite force, diet, and cranial morphology of fossil hominids. J. Hum. Evol. 17, 657–670 (1988).
doi: 10.1016/0047-2484(88)90023-1
Doden, E. & Halves, R. On the functional morphology of the human petrous bone. Am. J. Anat. 169, 451–462 (1984).
pubmed: 6731335
doi: 10.1002/aja.1001690407
Oxilia, G. et al. The physiological linkage between molar inclination and dental macrowear pattern. Am. J. Phys. Anthropol. 166, 941–951 (2018).
pubmed: 29633246
pmcid: 6120545
doi: 10.1002/ajpa.23476
Rathmann, H. & Reyes-Centeno, H. Testing the utility of dental morphological trait combinations for inferring human neutral genetic variation. Proc. Natl. Acad. Sci. 117, 10769–10777 (2020).
pubmed: 32376635
pmcid: 7245130
doi: 10.1073/pnas.1914330117
Alpaslan-Roodenberg, S. et al. Ethics of DNA research on human remains: Five globally applicable guidelines. Nature 599, 41–46 (2021).
pubmed: 34671160
pmcid: 7612683
doi: 10.1038/s41586-021-04008-x
Squires, K., Booth, T. & Roberts, C. A. The Ethics of Sampling Human Skeletal Remains for Destructive Analyses. In Ethical Approaches to Human Remains (eds Squires, K. et al.) 265–297 (Springer International Publishing, 2019).
doi: 10.1007/978-3-030-32926-6_12
Brown, K. E., Winter, B. J., Shen, C. & Yang, D. Y. Developing Minimally Destructive Protocols for DNA Analysis of Museum Collection Bone Artifacts. Saa 1 (2016).
Harney, É. et al. A minimally destructive protocol for DNA extraction from ancient teeth. Genome Res. 31, 472–483 (2021).
pubmed: 33579752
pmcid: 7919446
doi: 10.1101/gr.267534.120
Sirak, K. et al. Human auditory ossicles as an alternative optimal source of ancient DNA. Genome Res. 30, 427–436 (2020).
pubmed: 32098773
pmcid: 7111520
doi: 10.1101/gr.260141.119
Dobberstein, R. C. et al. Archaeological collagen: Why worry about collagen diagenesis?. Archaeol. Anthropol. Sci. 1, 31–42 (2009).
doi: 10.1007/s12520-009-0002-7
Poinar, H. N. & Stankiewicz, B. A. Protein preservation and DNA retrieval from ancient tissues. Proc. Natl. Acad. Sci. 96, 8426–8431 (1999).
pubmed: 10411891
pmcid: 17532
doi: 10.1073/pnas.96.15.8426
Scorrano, G. et al. Methodological strategies to assess the degree of bone preservation for ancient DNA studies. Ann. Hum. Biol. 42, 10–19 (2015).
pubmed: 25231926
doi: 10.3109/03014460.2014.954614
Fernández, E. et al. Aspartic acid racemization variability in ancient human remains: Implications in the prediction of ancient DNA recovery. J. Archaeol. Sci. 36, 965–972 (2009).
doi: 10.1016/j.jas.2008.11.009
Fredericks, J. D., Bennett, P., Williams, A. & Rogers, K. D. FTIR spectroscopy: A new diagnostic tool to aid DNA analysis from heated bone. Forensic Sci. Int. Genet. 6, 375–380 (2012).
pubmed: 21963795
doi: 10.1016/j.fsigen.2011.07.014
Gotherstrom, A., Collins, M. J., Angerbjorn, A. & Liden, K. Bone preservation and DNA amplification. Archaeometry 44, 395–404 (2002).
doi: 10.1111/1475-4754.00072
Kieser, J. A., Bernal, V., Neil Waddell, J. & Raju, S. The uniqueness of the human anterior dentition: A geometric morphometric analysis. J. Forensic Sci. 52, 671–677 (2007).
pubmed: 17397505
doi: 10.1111/j.1556-4029.2007.00403.x
Kontopoulos, I. et al. Screening archaeological bone for palaeogenetic and palaeoproteomic studies. PLoS One 15, 1–17 (2020).
doi: 10.1371/journal.pone.0235146
Leskovar, T., Zupanič Pajnič, I., Geršak, ŽM., Jerman, I. & Črešnar, M. ATR-FTIR spectroscopy combined with data manipulation as a pre-screening method to assess DNA preservation in skeletal remains. Forensic Sci. Int. Genet. 44, 102196 (2020).
pubmed: 31706110
doi: 10.1016/j.fsigen.2019.102196
Ottoni, C. et al. Preservation of ancient DNA in thermally damaged archaeological bone. Naturwissenschaften 96, 267–278 (2009).
pubmed: 19043689
doi: 10.1007/s00114-008-0478-5
Poinar, H. N., Höss, M., Bada, J. L. & Pääbo, S. Amino Acid Racemization and the Preservation of Ancient DNA. Science 272, 864–866 (1996).
pubmed: 8629020
doi: 10.1126/science.272.5263.864
Collins, M. J. et al. Is amino acid racemization a useful tool for screening for ancient DNA in bone?. Proc. R. Soc. B Biol. Sci. 276, 2971–2977 (2009).
doi: 10.1098/rspb.2009.0563
Gotherstrom, A., Collins, M. J., Angerbjorn, A. & Liden, K. Bone preservation and DNA amplification. Archaeometry 44, 395–404 (2002).
doi: 10.1111/1475-4754.00072
Haynes, S., Searle, J. B., Bretman, A. & Dobney, K. M. Bone preservation and ancient DNA: The application of screening methods for predicting DNA survival. J. Archaeol. Sci. 29, 585–592 (2002).
doi: 10.1006/jasc.2001.0731
Hedges, R. E. M. A review of current approaches in the pretreatment of bone. Radiocarbon 34, 279–291 (1992).
doi: 10.1017/S0033822200063438
Kirchner, M. T., Edwards, H. G. M., Lucy, D. & Pollard, A. M. Ancient and modern specimens of human teeth: A fourier transform Raman spectroscopic study. J. Raman Spectrosc. 28, 171–178 (1997).
doi: 10.1002/(SICI)1097-4555(199702)28:2/3<171::AID-JRS63>3.0.CO;2-V
Schwarz, C. et al. New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains. Nucleic Acids Res. 37, 3215–3229 (2009).
pubmed: 19321502
pmcid: 2691819
doi: 10.1093/nar/gkp159
Weiner, S. & Bar-Yosef, O. States of preservation of bones from prehistoric sites in the Near East: A survey. J. Archaeol. Sci. 17, 187–196 (1990).
doi: 10.1016/0305-4403(90)90058-D
Iuliani, P., Di Federico, L., Fontecchio, G. & Carlucci, G. RP-HPLC method with fluorescence detection for amino acids D/L ratio determination in fossil bones as a marker of DNA preservation. J. Sep. Sci. 33, 2411–2416 (2010).
pubmed: 20603838
doi: 10.1002/jssc.201000151
Collins, M. J., Waite, E. R. & Van Duin, A. C. T. Predicting protein decomposition: The case of aspartic-acid racemization kinetics. Philos. Trans. R. Soc. B Biol. Sci. 354, 51–64 (1999).
doi: 10.1098/rstb.1999.0359
Dobberstein, R. C., Huppertz, J., von Wurmb-Schwark, N. & Ritz-Timme, S. Degradation of biomolecules in artificially and naturally aged teeth: Implications for age estimation based on aspartic acid racemization and DNA analysis. Forensic Sci. Int. 179, 181–191 (2008).
pubmed: 18621493
doi: 10.1016/j.forsciint.2008.05.017
Fernández-Jalvo, Y., Pesquero, M. D. & Tormo, L. Now a bone, then calcite. Palaeogeogr. Palaeoclimatol. Palaeoecol. 444, 60–70 (2016).
doi: 10.1016/j.palaeo.2015.12.002
Wadsworth, C. et al. Comparing ancient DNA survival and proteome content in 69 archaeological cattle tooth and bone samples from multiple European sites. J. Proteomics 158, 1–8 (2017).
pubmed: 28095329
doi: 10.1016/j.jprot.2017.01.004
Dal Sasso, G. et al. Bone diagenesis variability among multiple burial phases at Al Khiday (Sudan) investigated by ATR-FTIR spectroscopy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 463, 168–179 (2016).
doi: 10.1016/j.palaeo.2016.10.005
Kendall, C., Eriksen, A. M. H., Kontopoulos, I., Collins, M. J. & Turner-Walker, G. Diagenesis of archaeological bone and tooth. Palaeogeogr. Palaeoclimatol. Palaeoecol. 491, 21–37 (2018).
doi: 10.1016/j.palaeo.2017.11.041
Kontopoulos, I. et al. Petrous bone diagenesis: A multi-analytical approach. Palaeogeogr. Palaeoclimatol. Palaeoecol. 518, 143–154 (2019).
doi: 10.1016/j.palaeo.2019.01.005
Lebon, M., Zazzo, A. & Reiche, I. Screening in situ bone and teeth preservation by ATR-FTIR mapping. Palaeogeogr. Palaeoclimatol. Palaeoecol. 416, 110–119 (2014).
doi: 10.1016/j.palaeo.2014.08.001
Carden, A. & Morris, M. D. Application of vibrational spectroscopy to the study of mineralized tissues (review). J. Biomed. Opt. 5, 259 (2000).
pubmed: 10958610
doi: 10.1117/1.429994
Chadefaux, C., Le Hô, A. S., Bellot-Gurlet, L. & Reiche, I. Curve-fitting micro-ATR-FTIR studies of the amide I and II bands of type I collagen in archaeological bone materials. e-PRESERVATIONScience 6, 129–137 (2009).
Doyle, B. B., Bendit, E. G. & Blout, E. R. Infrared spectroscopy of collagen and collagen-like polypeptides. Biopolymers 14, 937–957 (1975).
pubmed: 1156652
doi: 10.1002/bip.1975.360140505
Ishida, K. P. & Griffiths, P. R. Comparison of the amide I/II intensity ratio of solution and solid-state proteins sampled by transmission, attenuated total reflectance, and diffuse reflectance spectrometry. Appl. Spectrosc. 47, 584–589 (1993).
doi: 10.1366/0003702934067306
Vyskočilová, G., Ebersbach, M., Kopecká, R., Prokeš, L. & Příhoda, J. Model study of the leather degradation by oxidation and hydrolysis. Herit. Sci. 7, 1–13 (2019).
doi: 10.1186/s40494-019-0269-7
Goormaghtigh, E., Ruysschaert, J.-M. & Raussens, V. Evaluation of the information content in infrared spectra for protein secondary structure determination. Biophys. J. 90, 2946–2957 (2006).
pubmed: 16428280
pmcid: 1414549
doi: 10.1529/biophysj.105.072017
Barth, A. Infrared spectroscopy of proteins. Biochim. Biophys. Acta - Bioenerg. 1767, 1073–1101 (2007).
doi: 10.1016/j.bbabio.2007.06.004
Socrates, G. Infrared and Raman Characteristic Group Frequencies: Tables and Charts (John Wiley & Sons, 2004).
Fleet, M. E. Infrared spectra of carbonate apatites: ν2-Region bands. Biomaterials 30, 1473–1481 (2009).
pubmed: 19111895
doi: 10.1016/j.biomaterials.2008.12.007
Dal Sasso, G., Asscher, Y., Angelini, I., Nodari, L. & Artioli, G. A universal curve of apatite crystallinity for the assessment of bone integrity and preservation. Sci. Rep. 8, 1–13 (2018).
Pleshko, N. L., Boskey, A. L. & Mendelsohn, R. An FT-IR microscopic investigation of the effects of tissue preservation on bone. Calcif. Tissue Int. 51, 72–77 (1992).
pubmed: 1393781
doi: 10.1007/BF00296221
Nandiyanto, A. B. D., Oktiani, R. & Ragadhita, R. How to read and interpret ftir spectroscope of organic material. Indones. J. Sci. Technol. 4, 97–118 (2019).
doi: 10.17509/ijost.v4i1.15806
Martínez Cortizas, A. & López-Costas, O. Linking structural and compositional changes in archaeological human bone collagen: An FTIR-ATR approach. Sci. Rep. 10, 1–14 (2020).
doi: 10.1038/s41598-020-74993-y
Stani, C., Vaccari, L., Mitri, E. & Birarda, G. FTIR investigation of the secondary structure of type I collagen: New insight into the amide III band. Spectrochim. Acta - Part A Mol. Biomol. Spectrosc. 229, 118006 (2020).
doi: 10.1016/j.saa.2019.118006
Figueiredo, M. M., Gamelas, J. A. F. & Martins, A. G. Characterization of bone and bone-based graft materials using FTIR spectroscopy. Infrared Spectrosc. - Life Biomed. Sci. https://doi.org/10.5772/36379 (2012).
doi: 10.5772/36379
Ambrose, S. H. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 17, 431–451 (1990).
doi: 10.1016/0305-4403(90)90007-R
Naito, Y. I., Yamane, M. & Kitagawa, H. A protocol for using attenuated total reflection Fourier‐transform infrared spectroscopy for pre‐screening ancient bone collagen prior to radiocarbon dating. Rapid Commun. Mass Spectrom. https://doi.org/10.1002/rcm.8720 (2020).
doi: 10.1002/rcm.8720
pubmed: 31951673
Scaggion, C. et al. An FTIR-based model for the diagenetic alteration of archaeological bones. J. Archaeol. Sci. 161, 105900 (2024).
doi: 10.1016/j.jas.2023.105900
Ohi, M. D. EM analysis of protein structure. Encycl. Life Sci. https://doi.org/10.1002/9780470015902.a0021885 (2009).
doi: 10.1002/9780470015902.a0021885
Fietzek, P. P. & Kuehn, K. The primary structure of collagen. Int. Rev. Connect. Tissue Res. 7, 1–60 (1976).
pubmed: 177376
doi: 10.1016/B978-0-12-363707-9.50007-1
Prockop, D. J. & Williams, C. J. Structure of the Organic Matrix: Collagen Structure (Chemical). In Biological Mineralization and Demineralization (ed. Nancollas, G. H.) 161–177 (Springer Berlin Heidelberg, 1982). https://doi.org/10.1007/978-3-642-68574-3_8 .
doi: 10.1007/978-3-642-68574-3_8
DeFlores, L. P., Ganim, Z., Nicodemus, R. A. & Tokmakoff, A. Amide I′−II′ 2D IR spectroscopy provides enhanced protein secondary structural sensitivity. J. Am. Chem. Soc. 131, 3385–3391 (2009).
pubmed: 19256572
doi: 10.1021/ja8094922
Byler, D. M. & Susi, H. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25, 469–487 (1986).
pubmed: 3697478
doi: 10.1002/bip.360250307
Surewicz, W. K. & Mantsch, H. H. New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta – Protein Struct. Mol. Enzymol. 952, 115–130 (1988).
doi: 10.1016/0167-4838(88)90107-0
France, C. A. M., Thomas, D. B., Doney, C. R. & Madden, O. FT-Raman spectroscopy as a method for screening collagen diagenesis in bone. J. Archaeol. Sci. 42, 346–355 (2014).
doi: 10.1016/j.jas.2013.11.020
Riaz, T. et al. FTIR analysis of natural and synthetic collagen. Appl. Spectrosc. Rev. 53, 703–746 (2018).
doi: 10.1080/05704928.2018.1426595
Singh, B. R., DeOliveira, D. B., Fu, F.-N. & Fuller, M. P. Fourier transform infrared analysis of amide III bands of proteins for the secondary structure estimation. in Biomolecular Spectroscopy III (eds. Nafie, L. A. & Mantsch, H. H.) vol. 1890 47–55 (1993).
Unal, M., Jung, H. & Akkus, O. Novel Raman spectroscopic biomarkers indicate that postyield damage denatures bone’s collagen. J. Bone Miner. Res. 31, 1015–1025 (2016).
pubmed: 26678707
doi: 10.1002/jbmr.2768
Derrick, M. Evaluation of the state of degradation of Dead Sea Scroll samples using FT-IR spectroscopy. AIC B. Pap. Gr. Annu. 10, 1–16 (1991).
Piccolo, A. & Stevenson, F. J. Infrared spectra of Cu2+ Pb2+ and Ca2+ complexes of soil humic substances. Geoderma 27, 195–208 (1982).
doi: 10.1016/0016-7061(82)90030-1
Paschalis, E. P. et al. Spectroscopic characterization of collagen cross-links in bone. J. Bone Miner. Res. 16, 1821–1828 (2001).
pubmed: 11585346
doi: 10.1359/jbmr.2001.16.10.1821
Cappa, F., Paganoni, I., Carsote, C., Badea, E. & Schreiner, M. Studies on the effects of mixed light-thermal ageing on parchment by vibrational spectroscopy and micro hot table method. Herit. Sci. 8, 1–12 (2020).
doi: 10.1186/s40494-020-0353-z
Weiner, S. Microarchaeology. Beyond the visible archaeological record (Cambridge University Press, 2010).
doi: 10.1017/CBO9780511811210
Okazaki, M., Yoshida, Y., Yamaguchi, S., Kaneno, M. & Elliott, J. C. Affinity binding phenomena of DNA onto apatite crystals. Biomaterials 22, 2459–2464 (2001).
pubmed: 11516076
doi: 10.1016/S0142-9612(00)00433-6
Grunenwald, A. et al. Adsorption of DNA on biomimetic apatites: Toward the understanding of the role of bone and tooth mineral on the preservation of ancient DNA. Appl. Surf. Sci. 292, 867–875 (2014).
doi: 10.1016/j.apsusc.2013.12.063
Corrain, C., Capitanio, M. & Erspamer, G. I resti scheletrici della ne-cropoli di Salapia (Cerignola), secoli IX-III aC. Padova Soc. Coop. Tipogr. (1972).
Canci, A., Chavarria, A. & Marinato, M. Il cimitero della chiesa altomedievale di San Lorenzo di Desenzano (Bs). VI Congr. degli Archeol. Mediev. Ital. Note di Bi, 452–455 (2012).
Psycharis, V. et al. Chemical and X-ray diffraction peak broadening analysis, electron microscopy and IR studies of biological apatites. Mater. Sci. Forum 378–381, 759–764 (2001).
doi: 10.4028/www.scientific.net/MSF.378-381.759
Stathopoulou, E. T., Psycharis, V., Chryssikos, G. D., Gionis, V. & Theodorou, G. Bone diagenesis: New data from infrared spectroscopy and X-ray diffraction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 266, 168–174 (2008).
doi: 10.1016/j.palaeo.2008.03.022
Barth, H. D. et al. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials 32, 8892–8904 (2011).
pubmed: 21885114
pmcid: 4405888
doi: 10.1016/j.biomaterials.2011.08.013
De Campos Vidal, B. & Mello, M. L. S. Collagen type I amide I band infrared spectroscopy. Micron 42, 283–289 (2011).
doi: 10.1016/j.micron.2010.09.010
Mieczkowska, A. et al. Alteration of the bone tissue material properties in type 1 diabetes mellitus: A Fourier transform infrared microspectroscopy study. Bone 76, 31–39 (2015).
pubmed: 25813583
doi: 10.1016/j.bone.2015.03.010
Farlay, D. et al. The ratio 1660/1690 cm-1 measured by infrared microspectroscopy is not specific of enzymatic collagen cross-links in bone tissue. PLoS One 6, e28736 (2011).
pubmed: 22194900
pmcid: 3237494
doi: 10.1371/journal.pone.0028736
Paschalis, E. P., Mendelsohn, R. & Boskey, A. L. Infrared assessment of bone quality: A review. Clin. Orthop. Relat. Res. 469, 2170–2178 (2011).
pubmed: 21210314
pmcid: 3126953
doi: 10.1007/s11999-010-1751-4
Paschalis, E. P. et al. Bone fragility and collagen cross-links. J. Bone Miner. Res. 19, 2000–2004 (2004).
pubmed: 15537443
doi: 10.1359/jbmr.040820
Paschalis, E. P., Burr, D. B., Mendelsohn, R., Hock, J. M. & Boskey, A. L. Bone mineral and collagen quality in Humeri of ovariectomized cynomolgus monkeys given rhPTH(1–34) for 18 months. J. Bone Miner. Res. 18, 769–775 (2003).
pubmed: 12674338
doi: 10.1359/jbmr.2003.18.4.769
Savitzky, A. & Golay, M. J. E. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36, 1627–1639 (1964).
doi: 10.1021/ac60214a047
Arrondo, J. L. R., Muga, A., Castresana, J. & Goñi, F. M. Quantitative studies of the structure of proteins in solution by fourier-transform infrared spectroscopy. Prog. Biophys. Mol. Biol. 59, 23–56 (1993).
pubmed: 8419985
doi: 10.1016/0079-6107(93)90006-6
Ganim, Z. et al. Amide I two-dimensional infrared spectroscopy of proteins. Acc. Chem. Res. 41, 432–441 (2008).
pubmed: 18288813
doi: 10.1021/ar700188n
Schmidt, F. N. et al. Assessment of collagen quality associated with non-enzymatic cross-links in human bone using Fourier-transform infrared imaging. Bone 97, 243–251 (2017).
pubmed: 28109917
pmcid: 5443987
doi: 10.1016/j.bone.2017.01.015
Titus, J., Ghimire, H., Viennois, E., Didier Merlin, A. G. & Perera, U. Protein secondary structure analysis of dried blood serum using infrared spectroscopy to identify markers for colitis screening. J. Biophotonics https://doi.org/10.1002/jbio.201700057 (2018).
doi: 10.1002/jbio.201700057
pubmed: 28742273
Privat, K. L., O’connell, T. C. & Richards, M. P. Stable isotope analysis of human and faunal remains from the Anglo-Saxon cemetery at berinsfield, oxfordshire: Dietary and social implications. J. Archaeol. Sci. 29, 779–790 (2002).
doi: 10.1006/jasc.2001.0785
Richards, M. P. & Hedges, R. E. M. Stable isotope evidence for similarities in the types of marine foods used by late mesolithic humans at sites along the Atlantic coast of Europe. J. Archaeol. Sci. 26, 717–722 (1999).
doi: 10.1006/jasc.1998.0387
Harrison, R. G. & Katzenberg, M. A. Paleodiet studies using stable carbon isotopes from bone apatite and collagen: Examples from Southern Ontario and San Nicolas Island. California. J. Anthropol. Archaeol. 22, 227–244 (2003).
doi: 10.1016/S0278-4165(03)00037-0
Talamo, S., Fewlass, H., Maria, R. & Jaouen, K. “Here we go again”: The inspection of collagen extraction protocols for 14C dating and palaeodietary analysis. Sci. Technol. Archaeol. Res. 7, 62–77 (2021).
pubmed: 34381618
pmcid: 8300532
Guiry, E. J. & Szpak, P. Improved quality control criteria for stable carbon and nitrogen isotope measurements of ancient bone collagen. J. Archaeol. Sci. 132, 105416. https://doi.org/10.1016/j.jas.2021.105416 (2021).
Gaurav, K. A. & Patel, L. Machine Learning With R. (2020). doi: https://doi.org/10.4018/978-1-7998-2718-4.ch015 .
Kassambara, K. Machine Learning Essentials: Practical Guide in R. (CreateSpace Independent Publishing Platform, 2018).
Lane, D. M. Introduction to Statistics. Online Statistics Education: A Multimedia Course of Study (Rice University , University of Houston Clear Lake, and Tufts University, 2003). doi: https://doi.org/10.5005/jp/books/12176_6 .
Carrara, N., Scaggion, C. & Holland, E. The Tedeschi collection: A collection of documented and undocumented human skeletal remains at the Museum of Anthropology, Padua University (Italy). Am. J. Phys. Anthropol. 166, 930–933 (2018).
pubmed: 29607483
doi: 10.1002/ajpa.23471
Usai, D., Salvatori, S., Jakob, T. & David, R. The Al Khiday cemetery in central Sudan and its ‘classic/late Meroitic’ period graves. J. African Archaeol. 12, 183–204 (2014).
doi: 10.3213/2191-5784-10254
Usai, D. et al. Excavating a unique pre-Mesolithic cemetery in Central Sudan. Antiquity 84, 16–18 (2010).