Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-25T15:04:13.064Z Has data issue: false hasContentIssue false

Mineralization of Sialoliths Investigated by Ex Vivo and In Vivo X-ray Computed Tomography

Published online by Cambridge University Press:  04 February 2019

Pedro Nolasco*
Affiliation:
CeFEMA, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal IT, Department of Bioengineering, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
Paulo V. Coelho
Affiliation:
Service of Maxillofacial Surgery, Centro Hospitalar de Lisboa Central, R. José António Serrano 1150-199 Lisboa, Portugal NMS/FCM-UNL, Nova Medical School––Medical Sciences Faculty, Nova University of Lisbon, Campo Mártires da Pátria, 130, 1169-056 Lisboa, Portugal
Carla Coelho
Affiliation:
Service of Maxillofacial Surgery, Centro Hospitalar de Lisboa Central, R. José António Serrano 1150-199 Lisboa, Portugal
David F. Angelo
Affiliation:
NMS/FCM-UNL, Nova Medical School––Medical Sciences Faculty, Nova University of Lisbon, Campo Mártires da Pátria, 130, 1169-056 Lisboa, Portugal
J. R. Dias
Affiliation:
CDRsp, Polytechnic Institute of Leiria, Rua de Portugal, Zona Industrial, 2430-028, Marinha Grande, Portugal
Nuno M. Alves
Affiliation:
CDRsp, Polytechnic Institute of Leiria, Rua de Portugal, Zona Industrial, 2430-028, Marinha Grande, Portugal
António Maurício
Affiliation:
CERENA, Department of Civil Engineering, Architecture and Georessources, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
Manuel F.C. Pereira
Affiliation:
CERENA, Department of Civil Engineering, Architecture and Georessources, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
António P. Alves de Matos
Affiliation:
CESAM/CiiEM, Instituto Egas Moniz, Monte da Caparica, 2829-511 Caparica, Portugal
Raul C. Martins
Affiliation:
IT, Department of Bioengineering, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
Patrícia A. Carvalho
Affiliation:
CeFEMA, Instituto Superior Técnico, University of Lisbon, Av. Rovisco Pais, 1049-001 Lisboa, Portugal SINTEF Materials and Chemistry, Forskningsveien 1, 0373 Oslo, Norway
*
*Author for correspondence: Pedro Nolasco, E-mail: pedro.nolasco@tecnico.ulisboa.pt
Get access

Abstract

The fraction of organic matter present affects the fragmentation behavior of sialoliths; thus, pretherapeutic information on the degree of mineralization is relevant for a correct selection of lithotripsy procedures. This work proposes a methodology for in vivo characterization of salivary calculi in the pretherapeutic context. Sialoliths were characterized in detail by X-ray computed microtomography (μCT) in combination with atomic emission spectroscopy, Fourier transform infrared spectroscopy, X-ray diffraction, scanning electron microscopy, and transmission electron microscopy. Correlative analysis of the same specimens was performed by in vivo and ex vivo helical computed tomography (HCT) and ex vivo μCT. The mineral matter in the sialoliths consisted essentially of apatite (89 vol%) and whitlockite (11 vol%) with average density of 1.8 g/cm3. In hydrated conditions, the mineral mass prevailed with 53 ± 13 wt%, whereas the organic matter, with a density of 1.2 g/cm3, occupied 65 ± 10% of the sialoliths’ volume. A quantitative relation between sialoliths mineral density and X-ray attenuation is proposed for both HCT and μCT.

Type
Biological Science Applications
Copyright
Copyright © Microscopy Society of America 2019 

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.)

References

Alves de Matos, AP, Carvalho, PA, Almeida, A, Duarte, L, Vilar, R & Leitao, J (2007). On the structural diversity of sialoliths. Microsc Microanal 13, 390396.10.1017/S1431927607070754Google Scholar
Bazin, D, Daudon, M, Combes, C & Rey, C (2012). Characterization and some physicochemical aspects of pathological microcalcifications. Chem Rev 112, 50925120.Google Scholar
Blumenthal, NC, Betts, F & Posner, AS (1981). Formation and structure of Ca-deficient hydroxyapatite. Calcif Tissue Int 33, 111117.Google Scholar
Boskey, AL, Boyan-Salyers, BD, Burstein, LS & Mandel, ID (1981). Lipids associated with mineralization of human submandibular gland sialoliths. Arch Oral Biol 26, 779785.Google Scholar
Capaccio, P, Torretta, S, Ottavian, F, Sambataro, G & Pignataro, L (2007). Modern management of obstructive salivary diseases. Acta Otorhinolaryngol Ital 27, 161172.Google Scholar
Daudon, M, Donsimoni, R, Hennequin, C, Fellahi, S, Le Moel, G, Paris, M, Troupel, S & Lacour, B (1995). Sex- and age-related composition of 10 617 calculi analyzed by infrared spectroscopy. Urol Res 23, 319326.Google Scholar
Dorozhkin, SV (2003). Mechanism of solid-state conversion of non-stoichiometric hydroxyapatite to diphase calcium phosphate. Russ Chem Bull 52, 2639–2375.10.1023/B:RUCB.0000012357.20616.15Google Scholar
Dorozhkin, SV (2012). Calcium Orthophosphates: Applications in Nature, Biology, and Medicine. Singapore: Pan Stanford.10.1201/b12312Google Scholar
Escudier, MP, Brown, JE, Putcha, V, Capaccio, P & McGurk, M (2010). Factors influencing the outcome of extracorporeal shock wave lithotripsy in the management of salivary calculi. Laryngoscope 120, 15451549.Google Scholar
Feldkamp, LA, Davis, LC & Kress, JW (1984). Practical cone-beam algorithm. J Opt Soc Am A 1, 612619.Google Scholar
Geyer, LL, Schoepf, UJ, Meinel, FG, Nance, JW Jr., Bastarrika, G, Leipsic, JA, Paul, NS, Rengo, M, Laghi, A & De Cecco, CN (2015). State of the art: Iterative CT reconstruction techniques. Radiology 276, 339357.Google Scholar
Gomes, S, Renaudin, G, Mesbah, A, Jallot, E, Bonhomme, C, Babonneau, F & Nedelec, JM (2010). Thorough analysis of silicon substitution in biphasic calcium phosphate bioceramics: A multi-technique study. Acta Biomater 6, 32643274.Google Scholar
Gopal, R, Calvo, C, Ito, J & Sabine, WK (1974). Crystal structure of synthetic Mg-whitlockite, Ca18Mg2H2(PO4)14. Can J Chem 52, 11551164.Google Scholar
Grases, F, Santiago, C, Simonet, BM & Costa-Bauza, A (2003). Sialolithiasis: Mechanism of calculi formation and etiologic factors. Clin Chim Acta 334, 131136.Google Scholar
Habraken, WJ, Tao, J, Brylka, LJ, Friedrich, H, Bertinetti, L, Schenk, AS, Verch, A, Dmitrovic, V, Bomans, PH, Frederik, PM, Laven, J, van der Schoot, P, Aichmayer, B, de With, G, DeYoreo, JJ & Sommerdijk, NA (2013). Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate. Nat Commun 4, 1507.Google Scholar
Harrison, JD (2009). Causes, natural history, and incidence of salivary stones and obstructions. Otolaryngol Clin North Am 42, 927947.Google Scholar
Hasgall, PA, Di Gennaro, F, Baumgartner, C, Neufeld, E, Gosselin, MC, Payne, D, Klingenböck, A & Kuster, N (2015). IT'IS Database for thermal and electromagnetic parameters of biological tissues, Version 3.0.Google Scholar
Heimbach, D, Munver, R, Zhong, P, Jacobs, J, Hesse, A, Muller, SC & Preminger, GM (2000). Acoustic and mechanical properties of artificial stones in comparison to natural kidney stones. J Urol 164, 537544.Google Scholar
Ho, SP, Hsi, RCL, Yang, F, You, S, Killilea, D, Ramaswam, K, Chang, J, Chi, T & Stoller, M (2016). Kidney stones compared to dental calculi and salivary stones: Comparative analyses of mineral density and ultrastructure. J Urol 195, e778e779.Google Scholar
Jayasree, RS, Gupta, AK, Vivek, V & Nayar, VU (2008). Spectroscopic and thermal analysis of a submandibular sialolith of Wharton's duct resected using Nd:YAG laser. Lasers Med Sci 23, 125131.Google Scholar
Kalia, V, Kalra, G, Kaur, S & Kapoor, R (2015). CT scan as an essential tool in diagnosis of non-radiopaque sialoliths. J Maxillofac Oral Surg 14, 240244.Google Scholar
Koch, M, Schapher, M, Mantsopoulos, K, von Scotti, F, Goncalves, M & Iro, H (2017). Multimodal treatment in difficult sialolithiasis: Role of extracorporeal shock-wave lithotripsy and intraductal pneumatic lithotripsy. Laryngoscope 128, E332E338.Google Scholar
Kong, J & Yu, S (2007). Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sin (Shanghai) 39, 549559.Google Scholar
Kraus, W & Nolze, G (1996). POWDER CELL—a program for the representation and manipulation of crystal structures and calculation of the resulting X-ray powder patterns. J Appl Crystallogr 29, 301303.Google Scholar
Lambda, R, McGahan, JP, Corwin, MT, C-S, L, Tran, T, Seibert, JA & Boone, JM (2014). CT Hounsfield of soft tissues on unenhanced abdominal CT scans: Variability between two different manufacturers MDCT scanners. Genitourinary Imaging 203, 10131020.Google Scholar
LeGeros, RZ (1991). Calcium phosphates in oral biology and medicine. Monogr Oral Sci 15, 1201.Google Scholar
LeGeros, RZ, Sakae, T, Bautista, C, Retino, M & LeGeros, JP (1996). Magnesium and carbonate in enamel and synthetic apatites. Adv Dent Res 10, 225231.Google Scholar
Li, Y, Reid, GD, Bazin, D, Daudon, M & Duer, MJ (2016). Solid state NMR of salivary calculi: Proline-rich salivary proteins, citrate, polysaccharides, lipids, and organic–mineral interactions. C R Chim 19, 16651671.Google Scholar
Mahamid, J, Aichmayer, B, Shimoni, E, Ziblat, R, Li, C, Siegel, S, Paris, O, Fratzl, P, Weiner, S & Addadi, L (2010). Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays. Proc Natl Acad Sci USA 107, 63166321.Google Scholar
Movasaghi, Z, Rehman, S & Rehman, I (2008). Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl Spectrosc Rev 43, 134179.Google Scholar
Nguyen, QD & Daudon, M (1997). Infrared et Raman Spectra of Calculi. Paris: Elsevier.Google Scholar
Nolasco, P, Anjos, AJ, Marques, JM, Cabrita, F, da Costa, EC, Mauricio, A, Pereira, MF, de Matos, AP & Carvalho, PA (2013). Structure and growth of sialoliths: Computed microtomography and electron microscopy investigation of 30 specimens. Microsc Microanal 19, 11901203.Google Scholar
Nolasco, P, Dos Anjos, AJ, Dias, J, Coelho, PV, Coelho, C, Evaristo, M, Cavaleiro, A, Mauricio, A, Pereira, MFC, Infante, V, Alves de Matos, AP, Martins, RC & Carvalho, PA (2017). Local response of sialoliths to lithotripsy: Cues on fragmentation outcome. Microsc Microanal 23, 584598.Google Scholar
Otsu, N (1979). A threshold selection method from gray-level histograms. EEE Trans Syst Man Cybern Syst 9, 6266.Google Scholar
Patrick, S, Birur, NP, Gurushanth, K, Raghavan, AS & Gurudath, S (2017). Comparison of gray values of cone-beam computed tomography with Hounsfield units of multislice computed tomography: An in vitro study. Indian J Dent Res 28, 6670.Google Scholar
Prionas, ND, Ray, S & Boone, JM (2010). Volume assessment accuracy in computed tomography: A phantom study. J Appl Clin Med Phys 11, 3037.Google Scholar
Rehman, I & Bonfield, W (1997). Characterization of hydroxyapatite and carbonated apatite by photo acoustic FTIR spectroscopy. J Mater Sci Mater Med 8, 14.Google Scholar
Russel, G, Robertson, WG & Fleich, H (1973). Inhibitors of mineralization. In Biological Mineralization, Zipkin, I (Ed.), pp. 807825. New York, USA: John Wiley and Sons.Google Scholar
Rzymska-Grala, I, Stopa, Z, Grala, B, Golebiowski, M, Wanyura, H, Zuchowska, A, Sawicka, M & Zmorzynski, M (2010). Salivary gland calculi—contemporary methods of imaging. Pol J Radiol 75, 2537.Google Scholar
Sabot, JF, Gustin, MP, Delahougue, K, Faure, F, Machon, C & Hartmann, DJ (2012). Analytical investigation of salivary calculi, by mid-infrared spectroscopy. Analyst 137, 20952100.Google Scholar
Sakae, T, Yamamoto, H & Hirai, G (1981). Mode of occurrence of brushite and whitlockite in a sialolith. J Dent Res 60, 842844.Google Scholar
Saw, KC, McAteer, JA, Monga, AG, Chua, GT, Lingeman, JE & Williams, JC Jr. (2000). Helical CT of urinary calculi: Effect of stone composition, stone size, and scan collimation. AJR Am J Roentgenol 175, 329332.Google Scholar
Schrotzlmair, F, Muller, M, Pongratz, T, Eder, M, Johnson, T, Vogeser, M, von Holzschuher, V, Zengel, P & Sroka, R (2015). Laser lithotripsy of salivary stones: Correlation with physical and radiological parameters. Lasers Surg Med 47, 342349.Google Scholar
Seldin, HM, Seldin, SD & Rakower, W (1953). Conservative surgery for the removal of salivary calculi. Oral Surg Oral Med Oral Pathol 6, 579587.Google Scholar
Skinner, HCW (2005). Biominerals. Mineral Mag 69, 621641.Google Scholar
SkyScan, NV (2005). SkyScan 1172 Desktop X-ray Microtomography Instruction Maunual. Aartselaar: N.V SkyScan.Google Scholar
Slomiany, BL, Murty, VL, Aono, M, Slomiany, A & Mandel, ID (1982). Lipid composition of the matrix of human submandibular salivary gland stones. Arch Oral Biol 27, 673677.Google Scholar
Szalma, J, Boddi, K, Lempel, E, Sieroslawska, AF, Szabo, Z, Harfouche, R, Olasz, L, Takatsy, A & Guttman, A (2013). Proteomic and scanning electron microscopic analysis of submandibular sialoliths. Clin Oral Investig 17, 17091717.Google Scholar
Tatón, G, Rokita, E, Wróbel, A, Beckmann, F & Thor, P (2010). Renal calculi composition studies with the use of microtomography. Cent European J Urol 6, 8790.Google Scholar
Williams, JC Jr., Kim, SC, Zarse, CA, McAteer, JA & Lingeman, JE (2004). Progress in the use of helical CT for imaging urinary calculi. J Endourol 18, 937941.Google Scholar
Wopenka, B & Pasteris, J (2005). A mineralogical perspective on the apatite in bone. Mater Sci Eng 25, 131143.Google Scholar
Xie, B, Halter, TJ, Borah, BM & Nancollas, GH (2015). Aggregation of calcium phosphate and oxalate phases in the formation of renal stones. Cryst Growth Des 15, 204211.Google Scholar
Zarse, CA, McAteer, JA, Tann, M, Sommer, AJ, Kim, SC, Paterson, RF, Hatt, EK, Lingeman, JE, Evan, AP & Williams, JC Jr (2004). Helical computed tomography accurately reports urinary stone composition using attenuation values: In vitro verification using high-resolution micro-computed tomography calibrated to Fourier transform infrared microspectroscopy. Urology 63, 828833.Google Scholar
Zhu, P, Lin, Y, Lin, H, Xu, Y, Zheng, Q & Han, Y (2014). Computational fluid dynamics analysis of salivary flow and its effect on sialolithogenesis. Oral Dis 20, 624630.Google Scholar
Supplementary material: File

Nolasco et al. supplementary material

Appendix
Download Nolasco et al. supplementary material(File)
File 91.3 KB