Understanding heat-induced changes in human bone remains using ATR-FTIR combined with chemometrics

Abstract

Physical and chemical properties of skeletal bone undergo significant alterations during burning. The analysis of heat-induced changes in human skeletal remains has been providing important knowledge that has been applied to the research of burned bones from archaeological and forensic settings. The study of burned bones is also fundamental to understand funerary behaviors. To understand heat-induced crystallinity changes in human bones, remains from five medieval sites in Turkey: Hakemi Use, Komana, İznik, Oluz Höyük and Tasmasor were burned under controlled conditions (from 300 to 900°C). Attenuated Total Reflectance Fourier Transform Infrared spectroscopy (ATR-FTIR) combined with Principal Component Analysis (PCA) were used to analyze the findings. Clear spectral differences were observed in the organic and inorganic components of the bone remains as a function of the temperature. Approximate cremation temperatures of cremated remains from Acemhöyük in Turkey were estimated using Partial Least-Square Regression (PLS).

Keywords

• Archaeological bone remains
• Anatolia
• burned bones
• cremation
• crystallinity

References

1. Asscher Y, Regev L, Winer S, Boaretto E. (2011) Atomic disorder in fossil tooth and bone mineral: An FTIR study using the grinding curve method. Archeosciences 35: 135-140. https://doi.org/10.4000/archeosciences.3062
2. Bayarı Haman S. (2012) Applications of Vibrational Spectroscopy in Diagnosis and Screening of Dental Tissues. In: Severcan F, Haris PI (editors). Vibrational Spectroscopy in Diagnosis and Screening. IOS press.
3. Bayari Haman S, Özdemir K, Sen EH, Araujo-Andrade C, Erdal YS. (2020) Application of ATR-FTIR spectroscopy and chemometrics for the discrimination of human bone remains from different archaeological sites in Turkey. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 237: 118311. https://doi.org/10.1016/j.saa.2020.118311
4. Beasley M M, Bartelink E J, Taylor L, Miller R M. (2014) Comparison of transmission FTIR, ATR, and DRIFT spectra: implications for assessment of bone bioapatite diagenesis. Journal of Archaeological Science 46: 16-22. https://doi.org/10.1016/j.jas.2014.03.008
5. Boskey A, Mendelsohn R. (2005) Infrared analysis of bone in health and disease. Journal of Biomedical Optics 10(3): 031102. https://doi.org/10.1117/1.1922927
6. Boskey A, Pleshko Camacho N. (2007) FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 28 (15): 2465-2478. https://doi.org/10.1016/j.biomaterials.2006.11.043
7. Boskey AL, Coleman R. (2010) Aging and Bone. Journal of Dental Research 89 (12): 1333–1348. DOI: 10.1177/0022034510377791
8. Chadefaux C, Anne-Solenn LH, Bellot-Gurlet L, Reiche I. (2009) Curve- Fitting Micro –ATR- FTIR Studies of the Amide I and II Bands of Type I Collagen in Archaeological Bone Materials. E-Preservation Science 6: 129-137.

9. Dal Sasso G, Lebon M, Angelini I, Lara Maritan L, Usai D, Artiolo G. (2016) Bone diagenesis variability among multiple burial phases at Al Khiday (Sudan) investigated by ATR-FTIR spectroscopy. Palaeogeography Palaeoclimatology Palaeoecology 463: 168-179. https://doi.org/10.1016/j.palaeo.2016.10.005
10. Dal Sasso G, Asscher Y, Angelini I, Nodari L, Artioli G. (2018) A universal curve of apatite crystallinity for the assessment of bone integrity and preservation. Scientific Reports 8(1): 12025. https://doi.org/10.1038/s41598-018-30642-z
11. Dowker SEP, Elliott JC. (1979) Infrared absorption bands from NCO− and NCN2− in heated carbonate-containing apatites prepared in the presence of NH4+ ions. Calcified Tissue International 29 (1): 177-178. https://doi.org/10.1007/BF02408075
12. Durur M L. (2019) Acemhöyük ve Arıbaş Mezarlığı’ndan İnsan İskelet Kalıntılarının Gömü Geleneği Açısından İncelenmesi. MSc, Hacettepe Üniversitesi, Ankara, Turkey (Unpublished MA thesis, in Turkish with an abstract in English).
13. Efford M. (2016) The Implications of Thermogenic Modification for Anthropological Recovery of Burned Bone.
14. Ellingham STD, Thompson TJU, Islam M, Taylor G. (2015) Estimating temperature exposure of burnt bone-A methodological review. Science and Justice 55: 181-188. https://doi.org/10.1016/j.scijus.2014.12.002
15. Ellingham ST, Thompson TJ, Islam M. (2016) The Effect of Soft Tissue on Temperature Estimation from Burnt Bone Using Fourier Transform Infrared Spectroscopy. Journal of Forensic Sciences 61 (1): 153-159. https://doi.org/10.1111/1556-4029.12855
16. Elliott JC. (1994) Structure and Chemistry of the Apatites and Other Calcium Orthophosphates. Amsterdam, The Netherlands: Elsevier.
17. Elliot JC, Holcomb AW, Young RA. (1985) Infrared determination of the degree of substitution of hydroxyl by carbonate ions in human dental enamel. Calcified Tissue International 37(4): 372-375. https://doi.org/10.1007/BF02553704
18. Ekmen H. (2012) Acemhöyük’te Asur Ticaret Kolonileri Çağı Ölü Gömme Adetleri. Ph.D, Gazi Üniversitesi, Ankara, Turkey (Unpublished Ph.D thesis, in Turkish with an abstract in English).
19. Esbensen KH. (2005) Multivariate Data Analysis – In Practice. Esbjerg, Denmark: 5th Edition, CAMO Process AS.
20. Grandfield K, Vuong V, Schwarcz H P. (2018) Ultrastructure of Bone Hierarchical Features from Nanometer to Micrometer Scale Revealed in Focused Ion Beam Sections in the TEM. Calcified Tissue International 103(6): 606–616. https://doi.org/10.1007/s00223-018-0454-9
21. Gonçalves D, Vassalo AR, Mamede AP, Makhoul C, Piga G, Cunha E, Marques MPM, Batista de Carvalho LAE. (2018) Crystal clear: Vibrational spectroscopy reveals intrabone, intraskeleton, and interskeleton variation in human bones. American Journal of Physical Anthropology 166 (2): 296-312. https://doi.org/10.1002/ajpa.23430
22. Gonçalves D, Thompson TJU, Cunha E. (2011) Implications of heat-induced changes in bone on the interpretation of funerary behaviour and practice. Journal of Archaeological Science 38(6): 1308-1313. https://doi.org/10.1016/j.jas.2011.01.006
23. Grunenwald A, Keyser C, Sautereau AM, Crubezy E, Ludes B, Drouet C. (2014) Revisiting carbonate quantification in apatite (bio)minerals: a validated FTIR methodology. Journal of Archaeological Science 49: 134-141. https://doi.org/10.1016/j.jas.2014.05.004
24. Hedges REM. (2002) Bone diagenesis: an overview of processes. Archaeometry 44 (3): 319-328. https://doi.org/10.1111/1475-4754.00064
25. Holden JL, Phakey PP, Clement JG. (1995) Scanning electron microscope observations of heat-treated human bone. Forensic Science International 74 (1-2): 29-45. https://doi.org/10.1016/0379-0738(95)01735-2
26. Hollund HI, Ariese F, Fernandes R, Jans MME, Kars H. (2013) Testing an alternative high-throughput tool for investigating bone diagenesis: FTIR in attenuated total reflection (ATR) mode. Archaeometry 55 (3): 507-532. https://doi.org/10.1111/j.1475-4754.2012.00695.x
27. Kamış Y. (2012) Acemhöyük Erken Tunç Çağı Seramiği. Ph.D, Gazi Üniversitesi, Ankara, Turkey (Unpublished Ph. D thesis, in Turkish with an abstract in English).
28. Lebon M, Reiche I, Fröhlich F, Bahain JJ, Falguères C. (2008) Characterization of archaeological burnt bones: contribution of a new analytical protocol based on derivative FTIR spectroscopy and curve fitting of the v1 v3 PO4 domain. 392 (7): 1479-1488. https://doi.org/10.1007/s00216-008-2469-y
29. Lebon M, Reiche I, Bahain JJ, Chadefaux C, Moigne AM, Fröhlich F, Sémah F, Schwarcz HP, Falguère, C. (2010) New parameters for the characterization of diagenetic alterations and heat-induced changes of fossil bone mineral using Fourier transform infrared spectrometry. Journal of Archaeological Science 37 (9): 2265-2276. https://doi.org/10.1016/j.jas.2010.03.024
30. Lebon M, Müller K, Bellot-Gurlet L, Reche CP. (2011) Application des microspectrométries infrarouge et Raman à l'étude de s processus diagénéticques altérant les ossements paléollithiques. Archeosciences 35: 179-190. https://doi.org/10.4000/archeosciences.3114 (In French with an abstract in English).
31. Legan L, Leskovar T, Črešnar M, Cavalli F, Innocenti D, Ropret P. (2020) Non-invasive reflection FTIR characterization of archaeological burnt bones: Reference database and case studies. Journal of Cultural Heritage 41: 13-26. https://doi.org/10.1016/j.culher.2019.07.006
32. Lopes CCA, Limirio PHJO, Novais VR, Dechichi P. (2018) Fourier transform infrared spectroscopy (FTIR) application chemical characterization of enamel, dentin and bone, Applied Spectroscopy Review 53 (9): 747-769. https://doi.org/10.1080/05704928.2018.1431923
33. Mamede AP, Gonçalves D, Marques MPM, Batista de Carvalho LAE. (2017) Burned bones tell their own stories: A review of methodological approaches to assess heat-induced diagenesis. Applied Spectroscopy Review 53 (8): 603-635. https://doi.org/10.1080/05704928.2017.1400442
34. Marshall AO, Marshall CP. (2015) Vibrational spectroscopy of fossils. Palaeontology 58 (2): 201-211. https://doi.org/10.1111/pala.12144
35. Marques MPM, Mamede AP, Vassalo AR, Makhoul C, Cunha E, Gonçalves D, Parker SF, Batista de Carvalho LAE. (2018) Heat-induced Bone Diagenesis Probed by Vibrational Spectroscopy. Scientific Reports 8 (1): 1-13 https://doi.org/10.1038/s41598-018-34376-w
36. Munro LE, Longstaffe FJ, White C.D. (2007) Burning and boiling of modern deer bone: effects on crystallinity and oxygen isotope composition of bioapatite phosphate. Palaeogeograrphy Palaeoclimatology Palaoecology 249 (1-2): 90-102. https://doi.org/10.1016/j.palaeo.2007.01.011
37. GretagMacbeth. (2020) Munsell Soil Color Charts, Revised Washable Edition. GretagMacbeth, New Windsor, NY.
38. Nielsen-Marsh CM, Hedges REM. (2000) Patterns of Diagenesis in Bone I: The Effects of Site Environments. Journal of Archaeological Science 27 (12): 1139-1150. https://doi.org/10.1006/jasc.1999.0537
39. Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y., Kaufman MJ, Douglas EP, Gower LB. (2007) Bone structure and formation: A new perspective. Material Science Engineering 58: 77-116. https://doi.org/10.1016/j.mser.2007.05.001
40. Özgüç N. (1968) New Light on the Dating of the Levels of the Karum of Kanish and of Acemhöyük near Aksaray. American Journal of Archaeology 318-320.
41. Öztan A. (1991)1989 Yılı Acemhöyük Kazıları. KST/1 247-258.
42. Öztan A. (2014) 2013 Yılı Acemhöyük Kazıları ve Sonuçları. KST/2 61-72.
43. Person A, Bocherens H, Mariotti A, Renard M. (1996) Diagenetic evolution and experimental heating of bone phosphate. Palaeogeograrphy Palaeoclimatology Palaoecology 126: 135–149. https://doi.org/10.1016/S0031-0182(97)88906-7
44. Piga G, Gonçalves D, Thompson TJU, Brunetti A, Malgosa A, Enzo S. (2016) Understanding the Crystallinity Indices Behavior of Burned Bones and Teeth by ATR-IR and XRD in the Presence of Bioapatite Mixed with Other Phosphate and Carbonate Phases. International Journal of Spectroscopy Article ID 4810149. https://doi.org/10.1155/2016/4810149
45. Rey C, Renugopalakrishnan V, Collins B, Glimcher MJ. (1991) Fourier transform infrared spectroscopic study of the carbonate ions in bone mineral during aging. Calcified Tissue International 49: 251-258. https://doi.org/10.1007/BF02556214
46. Rey C, Combes C, Drouet C, Glimcher MJ. (2009) Osteoporos Bone mineral: update on chemical composition and structure. Osteoporosis International 20 (6): 1013-1021. https://doi.org/10.1007/s00198-009-0860-y
47. Rogers KD, Daniels P. (2002) An X-ray diffraction study of the effects of heat treatment on bone mineral microstructure. Biomaterials 23(12): 2577-2585. https://doi.org/10.1016/S0142-9612(01)00395-7
48. Roschger P, Paschalis EP, Fratzl P, Klaushofer K. (2008) Bone mineralization density distribution in health and disease. Bone 42 (3): 456-466. https://doi.org/10.1016/j.bone.2007.10.021
49. Snoeck C, Lee-Thorp JA, Schulting RJ. (2014) From bone to ash: Compositional and structural changes in burned modern and archaeological bone. Palaeogeograrphy Palaeoclimatology Palaoecology 416: 55-68. https://doi.org/10.1016/j.palaeo.2014.08.002
50. Stathopoulou ET, Psycharis V, Chryssikos GD, Gionis V, Theodorou G. (2008) Bone diagenesis: New data from infrared spectroscopy and X-ray diffraction. Palaeogeography Palaeoclimatology Palaeoecology 266 (3-4): 168-174. https://doi.org/10.1016/j.palaeo.2008.03.022
51. Stiner, MC, Kuhn ST, Weiner S, Bar-Yosef O. (1995) Differential burning, recrystallization, and fragmentation of archaeological bone. Journal of Archaeological Science 22 (2): 223-237. https://doi.org/10.1006/jasc.1995.0024
52. Surovell TA, Stiner MC. (2001) Standardizing infra-red measures of bone mineral crystallinity: an experimental approach. Journal of Archaeological Science 28 (6): 633-642. https://doi.org/10.1006/jasc.2000.0633
53. Thompson TJU, Chudek JA. (2007) A novel approach to the visualisation of heat induced structural change in bone. Science & Justice 47 (2): 99-104. https://doi.org/10.1016/j.scijus.2006.05.002
54. Thompson TJU, Gauthier M, Islam M. (2009) The application of a new method of Fourier Transform Infrared Spectroscopy to the analysis of burned bone. Journal of Archaeological Science 36 (3): 910-914. https://doi.org/10.1016/j.jas.2008.11.013
55. Thompson TJU, Islam M, Piduru K, Marcel A. (2011) An investigation into the internal and external variables acting on crystallinity index using Fourier transform infrared spectroscopy on unaltered and burned bone. Palaeogeograrphy Palaeoclimatology Palaoecology 299 (1-2): 168-74. https://doi.org/10.1016/j.palaeo.2010.10.044
56. Thompson TJU, Islam M, Bonniere M. (2013) A new statistical approach for determining the crystallinity of heat-altered bone mineral from FTIR spectra. Journal of Archaeological Science 40: 416-422. https://doi.org/10.1016/j.jas.2012.07.008
57. Trueman CN, Tuross N. (2002) Trace Elements in Recent and Fossil Bone Apatite. Reviews in Mineralogy and Geochemistry 48: 489-521. https://doi.org/10.2138/rmg.2002.48.13
58. Trueman CNG, Behrensmeyer AK, Tuross N, Weiner S. (2004) Mineralogical and compositional changes in bones exposed on soil surfaces in Amboseli National Park, Kenya: diagenetic mechanisms and the role of sediment pore fluids. Journal of Archaeological Science 31(6): 721-739. https://doi.org/10.1016/j.jas.2003.11.003
59. Ubelaker D H. (1989) Human Skeletal Remains: Excavation, Analysis, Interpretation (Manuals on Archeology, 2). Taraxacum, Washington.
60. Van Strydonck M, Boudin M, De Muller G. (2010) The Carbon Origin of Structural Carbonate in Bone Apatite of Cremated Bones, Radiocarbon 52 (2): 578-586. https://doi.org/10.1017/S0033822200045616
61. Von Euw S, Wang Y, Laurent G, Drouet C, Baboneau F, Nassif N, Azais T. (2019) Bone mineral: new insights into its chemical composition. Scientific Reports 9 (1): 1-11. https://doi.org/10.1038/s41598-019-44620-6
62. Weiner S, Bar-Josef O. (1990) States of preservation of bones from the prehistoric sites in the Near East: a survey. Journal of Archaeological Science 17 (2): 187-196. https://doi.org/10.1016/0305-4403(90)90058-D
63. Weiner S, Wagner HD. (1998) The material bone: Structure mechanical function relations. Annual Review of Materials Science 28 (1): 271-298. https://doi.org/10.1146/annurev.matsci.28.1.271
64. White TJ, Dong Z. (2003) Structural derivation and crystal chemistry of apatites. Acta Crystallographica Section B: Structural Science 59(1): 1-16. https://doi.org/10.1107/S0108768102019894
65. Wright LE, Schwarcz P. (1996) Infrared and isotopic evidence for diagenesis of bone apatite at Dos Pilas, Guatemala: palaeodietary implications. Journal of Archaeological Science 23 (6); 933-944. https://doi.org/10.1006/jasc.1996.0087
66. Zazzo A, Lebon, M, Chiotti L, Comby C, Delqué-Količ E, Nespoulet R, Reiche I. (2013) Can we Use Calcined Bones for 14C Dating the Paleolithic. Radiocarbon 55 (3): 1409-1421. https://doi.org/10.1017/S0033822200048347