Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-07-02T15:59:45.502Z Has data issue: false hasContentIssue false
  • English
  • Français

Carbonate and cation substitutions in hydroxylapatite in breast cancer micro-calcifications

Published online by Cambridge University Press:  11 March 2021

Yan Zhang Open the ORCID record for Yan Zhang [Opens in a new window] ,
Changqiu Wang ,
Yan Li ,
Anhuai Lu ,
Fanlu Meng ,
Hongrui Ding ,
Fang Mei ,
Jianying Liu ,
Kang Li  and
Chongqing Yang
...Show all authors
Yan Zhang
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Changqiu Wang
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Yan Li*
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Anhuai Lu*
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Fanlu Meng
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Hongrui Ding
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
Fang Mei
Affiliation:
Pathology Department, School of Basic Medical Science, Health Science Center of Peking University, Beijing100083, China
Jianying Liu
Affiliation:
Pathology Department, School of Basic Medical Science, Health Science Center of Peking University, Beijing100083, China
Kang Li
Affiliation:
Department of Cardiology, Beijing Hospital, Beijing100730, China
Chongqing Yang
Affiliation:
Department of Pathology, Beijing Hospital, Beijing100730, China
Jingyun Du
Affiliation:
Department of Pathology, Yidu Hospital of Traditional Chinese Medicine, Hubei, 443300, China
Yanzhang Li
Affiliation:
Key Laboratory of Orogenic Belts and Crustal Evolution, Beijing Key Laboratory of Mineral Environmental Function, School of Earth and Space Sciences, Peking University, Beijing100871, China
*
*Authors for correspondence: Yan Li, Email: [email protected]; Anhuai Lu, Email: [email protected]
*Authors for correspondence: Yan Li, Email: [email protected]; Anhuai Lu, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Calcification within breast cancer is a diagnostically significant radiological feature that generally consists of hydroxylapatite. Samples from 30 cases of breast carcinoma with calcification were investigated using optical microscopy, energy-dispersive X-ray analysis, transmission-electron microscopy, Fourier-transform infrared spectroscopy, Raman spectroscopy, synchrotron radiation X-ray diffraction and X-ray fluorescence. Under optical microscopy, the calcifications were found to consist of either irregular aggregates with widths > 200 μm or spherical aggregates similar to psammoma bodies with an average diameter of 30 μm. Transmission-electron microscopy showed that short columnar or dumbbell-shaped crystals with widths of 10–15 nm and lengths of 20–50 nm were the most common morphology; spherical aggregates (~1 μm in diameter) with amorphous coatings of fibrous nanocrystals were also observed. Results indicated that hydroxylapatite was the dominant mineral phase in the calcifications, and both CO32– and cation substitutions (Na, Mg, Zn, Fe, Sr, Cu and Mn) were present in the hydroxylapatite structure. Fourier-transform infrared spectra show peaks at 872 and 880 cm–1 indicating that CO32– substituted both the OH– (A type) and PO43– (B type) sites of hydroxylapatite, making it an A and B mixed type. The ratio of B- to A-type substitution was estimated in the range of 1.1–18.7 from the ratio of peak intensities (I872/I880), accompanied with CO32– contents from 1.1% to 14.5%. Trace arsenic, detected in situ by synchrotron radiation X-ray fluorescence was found to be distributed uniformly in the calcifications in the form of AsO43– substituting for PO43–. It is therefore proposed that identifying these trace elements in breast cancer calcifications may be promising for future clinical diagnostics.

Keywords

breast carcinomahydroxylapatitecarbonatebioapatiteisomorphic substitutiontrace elementB-type substitution
Type
Article
Information
Mineralogical Magazine , Volume 85 , Issue 3 , June 2021 , pp. 321 - 331
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Mineralogical Society of Great Britain and Ireland

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

The first two authors contributed equally to this paper.

Associate Editor: Runliang Zhu

References

Achal, V., Mukherjee, A., Kumari, D. and Zhang, Q. (2015) Biomineralization for sustainable construction – A review of processes and applications. Earth-Science Reviews, 148, 1–17.CrossRefGoogle Scholar
Antonakos, A., Liarokapis, E. and Leventouri, T. (2007) Micro-Raman and FTIR studies of synthetic and natural apatites. Biomaterials, 28, 3043–3054.CrossRefGoogle ScholarPubMed
Awonusi, A., Morris, M.D. and Tecklenburg, M.M. (2007) Carbonate assignment and calibration in the Raman spectrum of apatite. Calcified Tissue International, 81, 46–52.CrossRefGoogle ScholarPubMed
Baikie, T., Ng, G.M., Madhavi, S., Pramana, S.S., Blake, K., Elcombe, M. and White, T.J. (2009) The crystal chemistry of the alkaline-earth apatites A10(PO4)6CuxOy(H)z (A= Ca, Sr and Ba). Dalton Transactions, 34, 6722–6726.CrossRefGoogle Scholar
Baker, R., Rogers, K. D., Shepherd, N. and Stone, N. (2010) New relationships between breast microcalcifications and cancer. British Journal of Cancer, 103, 1034–1039.CrossRefGoogle ScholarPubMed
Baldassarre, F., Altomare, A., Corriero, N., Mesto, E., Lacalamita, M., Bruno, G., Sacchetti, A., Dida, B., Karaj, D., Ventura, G.D. et al. (2020) Crystal chemistry and luminescence properties of Eu-doped polycrystalline hydroxyapatite synthesized by chemical precipitation at room temperature. Crystals, 10, 250.CrossRefGoogle Scholar
Barralet, J., Best, S. and Bonfield, W. (1998) Carbonate substitution in precipitated hydroxyapatite: an investigation into the effects of reaction temperature and bicarbonate ion concentration. Journal of Biomedical Materials Research, 41, 79–86.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Belousova, E.A., Griffin, W.L., O'Reilly, S.Y. and Fisher, N.I. (2002) Apatite as an indicator mineral for mineral exploration: trace-element compositions and their relationship to host rock type. Journal of Geochemical Exploration, 76, 45–69.CrossRefGoogle Scholar
Blumenthal, N.C. and Posner, A.S. (1973) Hydroxyapatite: mechanism of formation and properties. Calcified Tissue Research, 13, 235–243.CrossRefGoogle ScholarPubMed
Blumenthal, N.C., Betts, F. and Posner, A.S. (1975) Effect of carbonate and biological macromolecules on formation and properties of hydroxyapatite. Calcified Tissue Research, 18, 81–90.10.1007/BF02546228CrossRefGoogle ScholarPubMed
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A. and Jemal, A. (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 68, 394–424.Google ScholarPubMed
Cheng, G., Zhang, Y., Yin, H., Ruan, Y., Sun, Y. and Lin, K. (2019) Effects of strontium substitution on the structural distortion of hydroxyapatite by Rietveld refinement and Raman Spectroscopy. Ceramics International, 45, 11073–11078.CrossRefGoogle Scholar
Cooke, M.M., McCarthy, G.M., Sallis, J.D. and Morgan, M.P. (2003) Phosphocitrate inhibits calcium hydroxyapatite induced mitogenesis and upregulation of matrix metalloproteinase-1, interleukin-1β and cyclooxygenase-2 mRNA in human breast cancer cell lines. Breast Cancer Research and Treatment, 79, 253–263.CrossRefGoogle ScholarPubMed
Cui, Y., Vogt, S., Olson, N., Glass, A.G. and Rohan, T.E. (2007) Levels of zinc, selenium, calcium, and iron in benign breast tissue and risk of subsequent breast cancer. Cancer Epidemiology and Prevention Biomarkers, 16, 1682–1685.CrossRefGoogle ScholarPubMed
Dorozhkin, S.V. and Epple, M. (2002) Biological and medical significance of calcium phosphates. Angewandte Chemie International Edition, 41, 3130–3146.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
El Feki, H., Savariault, J.M. and Salah, A.B. (1999) Structure refinements by the Rietveld method of partially substituted hydroxyapatite: Ca9Na0.5(PO4)4.5(CO3)1.5(OH)2. Journal of Alloys and Compounds, 287, 114–120.CrossRefGoogle Scholar
El Feki, H., Savariault, J.M., Salah, A.B. and Jemal, M. (2000) Sodium and carbonate distribution in substituted calcium hydroxyapatite. Solid State Sciences, 2, 577–586.CrossRefGoogle Scholar
Elliott, J.C. (2002) Calcium phosphate biominerals. Pp. 427–453 in: Phosphates (Kohn, M.L., Rakovan, J. and Hughes, J.M., editors) Reviews in Mineralogy and Geochemistry, 48. Mineralogical Society of America and the Geochemical Society, Washington DC.CrossRefGoogle Scholar
Fleet, M.E. (2009) Infrared spectra of carbonate apatites: ν2-Region bands. Biomaterials, 30, 1473–1481.CrossRefGoogle Scholar
Fleet, M.E. and Liu, X. (2003) Carbonate apatite type A synthesized at high pressure: new space group (P3) and orientation of channel carbonate ion. Journal of Solid State Chemistry, 174, 412–417.CrossRefGoogle Scholar
Fleet, M.E., Liu, X. and Liu, X. (2011) Orientation of channel carbonate ions in apatite: Effect of pressure and composition. American Mineralogist, 96, 1148–1157.CrossRefGoogle Scholar
Frappart, L., Remy, I., Lin, H.C., Bremond, A., Raudrant, D., Grousson, B. and Vauzelle, J.L. (1987) Different types of microcalcifications observed in breast pathology. Virchows Archiv A, 410, 179–187.CrossRefGoogle Scholar
Garola, R.E. and McGuire, W.L. (1978) A hydroxylapatite micromethod for measuring estrogen receptor in human breast cancer. Cancer Research, 38, 2216–2220.Google ScholarPubMed
Get'man, E.I., Loboda, S.N., Tkachenko, T.V., Yablochkova, N.V. and Chebyshev, K.A. (2010) Isomorphous substitution of samarium and gadolinium for calcium in hydroxyapatite structure. Russian Journal of Inorganic Chemistry, 55, 333–338.CrossRefGoogle Scholar
Gibson, I.R. and Bonfield, W. (2002) Novel synthesis and characterization of an AB-type carbonate-substituted hydroxyapatite. Journal of Biomedical Materials Research, 59, 697–708.CrossRefGoogle ScholarPubMed
Gosling, S., Scott, R., Greenwood, C., Bouzy, P., Nallala, J., Lyburn, I.D., Stone, N. and Rogers, K. (2019) Calcification microstructure reflects breast tissue microenvironment. Journal of Mammary Gland Biology and Neoplasia, 24, 333–342.CrossRefGoogle ScholarPubMed
Gross, K.A. and Berndt, C.C. (2002) Biomedical application of apatites. Pp. 631–672 in: Phosphates (Kohn, M.L., Rakovan, J. and Hughes, J.M., editors). Reviews in Mineralogy and Geochemistry, 48. Mineralogical Society of America and the Geochemical Society, Washington DC.CrossRefGoogle Scholar
Gülsün, M., Demirkazık, F.B. and Arıyürek, M. (2003) Evaluation of breast microcalcifications according to Breast Imaging Reporting and Data System criteria and Le Gal's classification. European Journal of Radiology, 47, 227–231.CrossRefGoogle ScholarPubMed
Haka, A.S., Shafer-Peltier, K.E., Fitzmaurice, M., Crowe, J., Dasari, R.R. and Feld, M.S. (2002) Identifying microcalcifications in benign and malignant breast lesions by probing differences in their chemical composition using Raman spectroscopy. Cancer Research, 62, 5375–5380.Google ScholarPubMed
Hammersley, A.P. (1997) FIT2D: An introduction and overview. ESRF Internal Rep. ESRF97HA02T, European Synchrotron Radiation Facility, Grenoble, France.Google Scholar
Hughes, J.M. and Rakovan, J.F. (2015) Structurally robust, chemically diverse: apatite and apatite supergroup minerals. Elements, 11, 165–170.CrossRefGoogle Scholar
Ito, A., Maekawa, K., Tsutsumi, S., Ikazaki, F. and Tateishi, T. (1997) Solubility product of OH-carbonated hydroxyapatite. Journal of Biomedical Materials Research, 36, 522–528.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Ivanova, T.I., Frank-Kamenetskaya, O.V., Kol'tsov, A.B. and Ugolkov, V.L. (2001) Crystal structure of calcium-deficient carbonated hydroxyapatite. Thermal decomposition. Journal of Solid State Chemistry, 160, 340–349.CrossRefGoogle Scholar
Jarcho, M., Bolen, C.H., Thomas, M.B., Bobick, J., Kay, J.F. and Doremus, R.H. (1976) Hydroxylapatite synthesis and characterization in dense polycrystalline form. Journal of Materials Science, 11, 2027–2035.CrossRefGoogle Scholar
Johnson, A.R., Armstrong, W.D. and Singer, L. (1966) Strontium incorporation into dental enamel. Science, 153, 1396–1397.CrossRefGoogle ScholarPubMed
Kaltenbach, B., Brandenbusch, V., Möbus, V., Mall, G., Falk, S., van den Bergh, M., Chevalier, F. and Müller-Schimpfle, M. (2017) A matrix of morphology and distribution of calcifications in the breast: analysis of 849 vacuum-assisted biopsies. European Journal of Radiology, 86, 221–226.CrossRefGoogle ScholarPubMed
Kato, K., Fukuzawa, K. and Mochizuki, Y. (2015) Modeling of hydroxyapatite-peptide interaction based on fragment molecular orbital method. Chemical Physics Letters, 629, 58–64.CrossRefGoogle Scholar
Kawasaki, T., Takahashi, S. and Ideda, K. (1985) Hydroxyapatite high-performance liquid chromatography: column performance for proteins. European Journal of Biochemistry, 152, 361–371.CrossRefGoogle ScholarPubMed
Krajewski, A., Mazzocchi, M., Buldini, P.L., Ravaglioli, A., Tinti, A., Taddei, P. and Fagnano, C. (2005) Synthesis of carbonated hydroxyapatites: efficiency of the substitution and critical evaluation of analytical methods. Journal of Molecular Structure, 744, 221–228.CrossRefGoogle Scholar
Kunitake, J.A., Choi, S., Nguyen, K.X., Lee, M.M., He, F., Sudilovsky, D., Morris, P.G., Jochelson, M.S., Hudis, C.A., Muller, D.A. et al. (2018) Correlative imaging reveals physiochemical heterogeneity of microcalcifications in human breast carcinomas. Journal of Structural Biology, 202, 25–34.CrossRefGoogle ScholarPubMed
Lala, S., Ghosh, M., Das, P.K., Das, D., Kar, T. and Pradhan, S.K. (2016) Magnesium substitution in carbonated hydroxyapatite: structural and microstructural characterization by Rietveld's refinement. Materials Chemistry and Physics, 170, 319–329.CrossRefGoogle Scholar
Larner, F., Woodley, L.N., Shousha, S., Moyes, A., Humphreys-Williams, E., Strekopytov, S., Halliday, A.N., Rehkämper, M. and Coombes, R.C. (2015) Zinc isotopic compositions of breast cancer tissue. Metallomics, 7, 112–117.CrossRefGoogle ScholarPubMed
Legeros, R.Z., Trautz, O.R., Legeros, J.P., Klein, E. and Shirra, W.P. (1967) Apatite crystallites: effects of carbonate on morphology. Science, 155, 1409–1411.CrossRefGoogle ScholarPubMed
LeGeros, R.Z., Trautz, O.R., Klein, E. and LeGeros, J.P. (1969) Two types of carbonate substitution in the apatite structure. Experientia, 25, 5–7.CrossRefGoogle ScholarPubMed
LeGeros, R.Z., Miravite, M.A., Quirolgico, G.B. and Curzon, M.E.J. (1976) The effect of some trace elements on the lattice parameters of human and synthetic apatites. Calcified Tissue Research, 22, 362–367.CrossRefGoogle Scholar
Li, Z. and Pasteris, J.D. (2014) Chemistry of bone mineral, based on the hypermineralized rostrum of the beaked whale Mesoplodon densirostris. American Mineralogist, 99, 645–653.CrossRefGoogle ScholarPubMed
Li, Z.Y., Lam, W.M., Yang, C., Xu, B., Ni, G.X., Abbah, S.A., Cheung, K.M.C., Luk, K.D.K. and Lu, W.W. (2007) Chemical composition, crystal size and lattice structural changes after incorporation of strontium into biomimetic apatite. Biomaterials, 28, 1452–1460.CrossRefGoogle ScholarPubMed
Liberman, L., Abramson, A.F., Squires, F.B., Glassman, J.R., Morris, E.A. and Dershaw, D.D. (1998) The breast imaging reporting and data system: positive predictive value of mammographic features and final assessment categories. AJR. American Journal of Roentgenology, 171, 35–40.CrossRefGoogle ScholarPubMed
Maaroufi, Y., Lacroix, M., Lespagnard, L., Journé, F., Larsimont, D. and Leclercq, G. (2000) Estrogen receptor of primary breast cancers: evidence for intracellular proteolysis. Breast Cancer Research, 2, 1–11.CrossRefGoogle ScholarPubMed
Madupalli, H., Pavan, B. and Tecklenburg, M.M. (2017) Carbonate substitution in the mineral component of bone: Discriminating the structural changes, simultaneously imposed by carbonate in A and B sites of apatite. Journal of Solid State Chemistry, 255, 27–35.CrossRefGoogle Scholar
Mangialardo, S., Cottignoli, V., Cavarretta, E., Salvador, L., Postorino, P. and Maras, A. (2012) Pathological biominerals: Raman and infrared studies of bioapatite deposits in human heart valves. Applied Spectroscopy, 66, 1121–1127.CrossRefGoogle ScholarPubMed
Matsunaga, K., Murata, H., Mizoguchi, T. and Nakahira, A. (2010) Mechanism of incorporation of zinc into hydroxyapatite. Acta Biomaterialia, 6, 2289–2293.CrossRefGoogle ScholarPubMed
McConnell, D. (1960) The stoichiometry of hydroxyapatite. Naturwissenschaften, 47, 227–227.CrossRefGoogle Scholar
Merry, J.C., Gibson, I.R., Best, S.M. and Bonfield, W. (1998) Synthesis and characterization of carbonate hydroxyapatite. Journal of Materials Science, 9, 779–783.Google ScholarPubMed
Mills, S.J. and Christy, A.G. (2016) The Great Barrier Reef Expedition 1928–29: The crystal structure and occurrence of weddellite, ideally CaC2O4⋅2.5H2O, from the Low Isles, Queensland. Mineralogical Magazine, 80, 399–406.CrossRefGoogle Scholar
Morgan, M.P., Cooke, M.M., Christopherson, P.A., Westfall, P.R. and McCarthy, G.M. (2001) Calcium hydroxyapatite promotes mitogenesis and matrix metalloproteinase expression in human breast cancer cell lines. Molecular Carcinogenesis, 32, 111–117.CrossRefGoogle ScholarPubMed
Nelson, D.G. and Featherstone, J.D. (1982) Preparation, analysis, and characterization of carbonated apatites. Calcified Tissue International, 34, S69–81.Google ScholarPubMed
Nemliher, J.G., Baturin, G.N., Kallaste, T.E. and Murdmaa, I.O. (2004) Transformation of hydroxyapatite of bone phosphate from the ocean bottom during fossilization. Lithology and Mineral Resources, 39, 468–479.CrossRefGoogle Scholar
Ng, K., Looi, L. and Bradley, D. (1997) The elemental composition of breast tissue: Can this be related to breast particle deposition? Journal of Radioanalytical and Nuclear Chemistry, 217, 193–199.CrossRefGoogle Scholar
Obadia, L., Amador, G., Daculsi, G. and Bouler, J.M. (2003) Calcium-deficient apatite: influence of granule size and consolidation mode on release and in vitro activity of vancomycin. Biomaterials, 24, 1265–1270.CrossRefGoogle ScholarPubMed
Obenauer, S., Hermann, K.P. and Grabbe, E. (2005) Applications and literature review of the BI-RADS classification. European Radiology, 15, 1027–1036.CrossRefGoogle ScholarPubMed
Ou-Yang, H., Paschalis, E.P., Mayo, W.E., Boskey, A.L. and Mendelsohn, R. (2001) Infrared microscopic imaging of bone: spatial distribution of CO32−. Journal of Bone and Mineral Research, 16, 893–900.CrossRefGoogle Scholar
Pan, Y. and Fleet, M.E. (2002) Compositions of the apatite-group minerals: substitution mechanisms and controlling factors. Pp. 13–49 in: Phosphates (Kohn, M.L., Rakovan, J. and Hughes, J.M., editors). Reviews in Mineralogy and Geochemistry, 48. Mineralogical Society of America and the Geochemical Society, Washington DC.CrossRefGoogle Scholar
Panko, W.B., Watson, C.S. and Clark, J.H. (1981) The presence of a second, specific estrogen binding site in human breast cancer. Journal of Steroid Biochemistry, 14, 1311–1316.CrossRefGoogle ScholarPubMed
Pasero, M., Kampf, A.R., Ferraris, C., Pekov, I.V., Rakovan, J. and White, T.J. (2010) Nomenclature of the apatite supergroup minerals. European Journal of Mineralogy, 22, 163–179.CrossRefGoogle Scholar
Penel, G., Leroy, G., Rey, C. and Bres, E. (1998) MicroRaman spectral study of the PO4 and CO3 vibrational modes in synthetic and biological apatites. Calcified Tissue International, 63, 475–481.CrossRefGoogle ScholarPubMed
Peroos, S., Du, Z. and de Leeuw, N.H. (2006) A computer modelling study of the uptake, structure and distribution of carbonate defects in hydroxy-apatite. Biomaterials, 27, 2150–2161.CrossRefGoogle ScholarPubMed
Raynaud, S., Champion, E., Bernache-Assollant, D. and Thomas, P. (2002) Calcium phosphate apatites with variable Ca/P atomic ratio I. Synthesis, characterisation and thermal stability of powders. Biomaterials, 23, 1065–1072.CrossRefGoogle ScholarPubMed
Rimola, A., Corno, M., Zicovich-Wilson, C.M. and Ugliengo, P. (2009) Ab initio modeling of protein/biomaterial interactions: competitive adsorption between glycine and water onto hydroxyapatite surfaces. Physical Chemistry Chemical Physics, 11, 9005–9007.CrossRefGoogle ScholarPubMed
Romaniuk, A.M., Lyndin, M.S., Moskalenko, R.A., Hortynska, O.M. and Lyndina, Y.M. (2016) The role of heavy metal salts in pathological biomineralization of breast cancer tissue. Advances in Clinical and Experimental Medicine, 25, 907–910CrossRefGoogle Scholar
Sathyavathi, R., Saha, A., Soares, J.S., Spegazzini, N., McGee, S., Dasari, R.R., Fitzmaurice, M and Barman, I. (2015) Raman spectroscopic sensing of carbonate intercalation in breast microcalcifications at stereotactic biopsy. Scientific Reports, 5, 1–12.CrossRefGoogle ScholarPubMed
Saul, J.M. (2009) Did detoxification processes cause complex life to emerge? Lethaia, 42, 179–184.CrossRefGoogle Scholar
Scimeca, M., Bischetti, S., Lamsira, H.K., Bonfiglio, R. and Bonanno, E. (2018) Energy Dispersive X-ray (EDX) microanalysis: A powerful tool in biomedical research and diagnosis. European Journal of Histochemistry: EJH, 62, 2841Google ScholarPubMed
Seredin, P., Goloshchapov, D., Prutskij, T. and Ippolitov, Y. (2015) Phase transformations in a human tooth tissue at the initial stage of caries. PLoS One, 10, e0124008.CrossRefGoogle Scholar
Shen, Y., Liu, J., Lin, K. and Zhang, W. (2012) Synthesis of strontium substituted hydroxyapatite whiskers used as bioactive and mechanical reinforcement material. Materials Letters, 70, 76–79.CrossRefGoogle Scholar
Solé, V.A., Papillon, E., Cotte, M., Walter, P. and Susini, J.A. (2007) A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochimica Acta, B62, 63–68.CrossRefGoogle Scholar
Szuszkiewicz, A., Pieczka, A., Gołębiowska, B., Dumańska-Słowik, M., Marszałek, M. and Szełęg, E. (2018) Chemical composition of Mn-and Cl-rich apatites from the Szklary pegmatite, Central Sudetes, SW Poland: Taxonomic and genetic implications. Minerals, 8, 350.CrossRefGoogle Scholar
Tanwell, C.S., Gescher, A., Bradshaw, T.D. and Pettit, G.R. (1994) The role of protein kinase C isoenzymes in the growth inhibition caused by bryostatin 1 in human A549 lung and MCF-7 breast carcinoma cells. International Journal of Cancer, 56, 585–592.CrossRefGoogle Scholar
Tarasevich, Y.I., Shkutkova, E.V. and Janusz, W. (2012) Sorption of ions of heavy metals from aqueous solutions on hydroxylapatite. Journal of Water Chemistry and Technology, 34, 125–132.CrossRefGoogle Scholar
Vignoles, M., Bonel, G., Holcomb, D.W. and Young, R.A. (1988) Influence of preparation conditions on the composition of type B carbonated hydroxyapatite and on the localization of the carbonate ions. Calcified Tissue International, 43, 33–40.CrossRefGoogle ScholarPubMed
Wang, C., Yang, R., Li, Y., Xiong, C., Zhao, W., Liu, J., Zhang, B. and Lu, A. (2011) A study on psammoma body mineralization in meningiomas. Journal of Mineralogical and Petrological Sciences, 106, 229–234.CrossRefGoogle Scholar
Wang, M., Qian, R., Bao, M., Gu, C. and Zhu, P. (2018) Raman, FTIR and XRD study of bovine bone mineral and carbonated apatites with different carbonate levels. Materials Letters, 210, 203–206.CrossRefGoogle Scholar
Webster, T.J., Ergun, C., Doremus, R.H. and Bizios, R. (2002) Hydroxylapatite with substituted magnesium, zinc, cadmium, and yttrium. II. Mechanisms of osteoblast adhesion. Journal of Biomedical Materials Research, 59, 312–317.CrossRefGoogle ScholarPubMed
Weiner, S. and Dove, P.M. (2003) An overview of biomineralization processes and the problem of the vital effect. Pp. 1–29 in: Biomineralisation (Dove, P.M., Weiner, S. and De Yoreo, J.J., editors). Reviews in Mineralogy and Geochemistry, 54. Mineralogical Society of America and the Geochemical Society, Washington DC.Google Scholar
White, T.J. and Dong, Z. (2003) Structural derivation and crystal chemistry of apatites. Acta Crystallographica, B59, 1–16.Google Scholar
World Health Organization (2017) Guide to cancer early diagnosis. World Health Organization. https://apps.who.int/iris/handle/10665/254500.Google Scholar
Yücel, I., Arpaci, F., Özet, A., Döner, B., Karayilanoĝlu, T., Sayar, A. and Berk, Ö. (1994) Serum copper and zinc levels and copper/zinc ratio in patients with breast cancer. Biological Trace Element Research, 40, 31–38.CrossRefGoogle ScholarPubMed