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Journal of Imaging Informatics in Medicine

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07-09-2022 | Tooth Extraction | Original Paper

Definition of the Region of Interest for the Assessment of Alveolar Bone Repair Using Micro-computed Tomography

Authors: Juliana Simeão Borges, Vitor Cardoso Costa, Milena Suemi Irie, Gabriella Lopes de Rezende Barbosa, Rubens Spin-Neto, Priscilla Barbosa Ferreira Soares

Published in: Journal of Imaging Informatics in Medicine | Issue 1/2023

Abstract

The objective of this study was to evaluate the influence of the extraction socket (distal or lingual root) and the type of region of interest (ROI) definition (manual or predefined) on the assessment of alveolar repair following tooth extraction using micro-computed tomography (micro-CT). The software package used for scanning, reconstruction, reorientation, and analysis of images (NRecon^®, DataViewer^®, CT-Analyzer^®) was acquired through Bruker < https://www.bruker.com > . The sample comprised the micro-CT volumes of seven Wistar rat mandibles, in which the right first molar was extracted. The reconstructed images were analyzed using the extraction sockets, i.e., the distal and intermediate lingual root and the method of ROI definition: manual (MA), central round (CR), and peripheral round (PR). The bone volume fraction (BV/TV) values obtained were analyzed by two-way ANOVA with Tukey’s post hoc test (α = 5%). The distal extraction socket resulted in significantly lower BV/TV values than the intermediate lingual socket for MA (P = 0.001), CR (P < 0.001), and PR (P < 0.001). Regarding the ROI, when evaluating the distal extraction socket, the BV/TV was significantly higher (P < 0.001) for MA than for CR and PR, with a lower BV/TV for CR. However, no significant difference was observed for MA (P = 0.855), CR (P = 0.769), or PR (P = 0.453) in the intermediate lingual extraction socket. The bone neoformation outcome (BV/TV) for alveolar bone repair after tooth extraction is significantly influenced by the ROI and the extraction socket. Using the predefined method with a standardized ROI in the central region of the distal extraction socket resulted in the assessment of bone volume, demonstrating the most critical region of the bone neoformation process.

Javed A, Chen H, Ghori FY: Genetic and transcriptional control of bone formation. Oral Maxillofac Surg Clin North Am 22(3): 283-293, 2010. https://doi.org/10.1016/j.coms.2010.05.001.CrossRefPubMedPubMedCentral

Pagni G, Pellegrini G, Giannobile WV, Rasperini G: Postextraction alveolar ridge preservation: biological basis and treatments. Int J Dent 2012: 151030, 2012. https://doi.org/10.1155/2012/151030.CrossRefPubMedPubMedCentral

Haworth S, Shungin D, Kwak SY, Kim HY, West NX, Thomas SJ, Franks PW, Timpson NJ, Shin MJ, Johansson I: Tooth loss is a complex measure of oral disease: Determinants and methodological considerations. Community Dent Oral Epidemiol 46(6): 555-562, 2018. https://doi.org/10.1111/cdoe.12391.CrossRefPubMedPubMedCentral

Calixto RF, Teófilo JM, Brentegani LG, Lamano-Carvalho TL: Grafting of tooth extraction socket with inorganic bovine bone or bioactive glass particles: comparative histometric study in rats. Implant Dent 16(3): 260-269, 2007. https://doi.org/10.1097/ID.0b013e3180500b95.CrossRefPubMed

Lin Z, Rios HF, Volk SL, Sugai JV, Jin Q, Giannobile WV: Gene expression dynamics during bone healing and osseointegration. J Periodontol 82(7): 1007-1017, 2011. https://doi.org/10.1902/jop.2010.100577.CrossRefPubMed

Hassumi JS, Mulinari-Santos G, Fabris ALDS, Jacob RGM, Gonçalves A, Rossi AC, Freire AR, Faverani LP, Okamoto R: Alveolar bone healing in rats: micro-CT, immunohistochemical and molecular analysis. J Appl Oral Sci 18; 26:e20170326, 2018. https://doi.org/10.1590/1678-7757-2017-0326.

Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R: Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25: 1468-1486, 2010.CrossRefPubMed

Kruse C, Spin-Neto R, Reibel J, Wenzel A, Kirkevang LL: Diagnostic validity of periapical radiography and CBCT for assessing periapical lesions that persist after endodontic surgery. Dentomaxillofac Radiol 46(7): 20170210, 2017. https://doi.org/10.1259/dmfr.20170210.CrossRefPubMedPubMedCentral

Irie MS, Rabelo GD, Spin-Neto R, Dechichi P, Borges JS, Soares PBF: Use of micro-computed tomography for bone evaluation in dentistry. Braz Dent J 29(3): 227-238, 2018. https://doi.org/10.1590/0103-6440201801979.CrossRefPubMed

10.

Van 't Hof RJ, Dall'Ara E: Analysis of bone architecture in rodents using micro-computed tomography. Methods Mol Biol 1914: 507-531, 2019. https://doi.org/10.1007/978-1-4939-8997-3_28.CrossRef

11.

Gaêta-Araujo H, Nascimento EHL, Brasil DM, Madlum DV, Haiter-Neto F, Oliveira-Santos C: Influence of reconstruction parameters of micro-computed tomography on the analysis of bone mineral density. Imaging Sci Dent 50(2): 153-159, 2020. https://doi.org/10.5624/isd.2020.50.2.153.CrossRefPubMedPubMedCentral

12.

Chavez MB, Chu EY, Kram V, de Castro LF, Somerman MJ, Foster BL: Guidelines for micro-computed tomography analysis of rodent dentoalveolar tissues. JBMR Plus 5(3): e10474, 2021. https://doi.org/10.1002/jbm4.10474.CrossRefPubMedPubMedCentral

13.

Mashiatulla M, Ross RD, Sumner DR: Validation of cortical bone mineral density distribution using micro-computed tomography. Bone 99: 53-61, 2017. https://doi.org/10.1016/j.bone.2017.03.049.CrossRefPubMedPubMedCentral

14.

Suttapreyasri S, Suapear P, Leepong N: The accuracy of cone-beam computed tomography for evaluating bone density and cortical bone thickness at the implant site: Micro-computed tomography and histologic analysis. J Craniofac Surg 29(8): 2026-2031, 2018. https://doi.org/10.1097/SCS.0000000000004672.CrossRefPubMed

15.

Chen CH, Wang L, Serdar Tulu U, Arioka M, Moghim MM, Salmon B, Chen CT, Hoffmann W, Gilgenbach J, Brunski JB, Helms JA: An osteopenic/osteoporotic phenotype delays alveolar bone repair. Bone 112: 212-219, 2018. https://doi.org/10.1016/j.bone.2018.04.019.CrossRefPubMed

16.

de Oliveira Puttini I, Gomes-Ferreira PHDS, de Oliveira D, Hassumi JS, Gonçalves PZ, Okamoto R: Teriparatide improves alveolar bone modelling after tooth extraction in orchiectomized rats. Arch Oral Biol 102: 147-154, 2019. https://doi.org/10.1016/j.archoralbio.2019.04.007.CrossRefPubMed

17.

Só BB, Silveira FM, Llantada GS, Jardim LC, Calcagnotto T, Martins MAT, Martins MD: Effects of osteoporosis on alveolar bone repair after tooth extraction: A systematic review of preclinical studies. Arch Oral Biol 125: 105054, 2021. https://doi.org/10.1016/j.archoralbio.2021.105054.CrossRefPubMed

18.

Christiansen BA: Effect of micro-computed tomography voxel size and segmentation method on trabecular bone microstructure measures in mice. Bone Rep 5: 136-140, 2016. https://doi.org/10.1016/j.bonr.2016.05.006.CrossRefPubMedPubMedCentral

19.

Djomehri SI, Candell S, Case T, Browning A, Marshall GW, Yun W, Lau SH, Webb S, Ho SP: Mineral density volume gradients in normal and diseased human tissues. PLoS One 10(4): e0121611, 2015. https://doi.org/10.1371/journal.pone.0121611.CrossRefPubMedPubMedCentral

20.

Kalatzis-Sousa NG, Spin-Neto R, Wenzel A, Tanomaru-Filho M, Faria G: Use of micro-computed tomography for the assessment of periapical lesions in small rodents: a systematic review. Int Endod J 50(4): 352-366, 2017. https://doi.org/10.1111/iej.12633.CrossRefPubMed

21.

Yamasaki MC, Nejaim Y, Roque-Torres GD, Freitas DQ: Meloxicam as a radiation-protective agent on mandibles of irradiated rats. Braz Dent J 28(2): 249-255, 2017. https://doi.org/10.1590/0103-6440201701271.CrossRefPubMed

22.

Yang S, Zhu L, Xiao L, Shen Y, Wang L, Peng B, Haapasalo M: Imbalance of interleukin-17+ T-cell and Foxp3+ regulatory T-cell dynamics in rat periapical lesions. J Endod 40(1): 56-62, 2014. https://doi.org/10.1016/j.joen.2013.09.033.CrossRefPubMed

23.

Chen Y, Guo Y, Li J, Chen YY, Liu Q, Tan L, Gao ZR, Zhang SH, Zhou YH, Feng YZ: Endoplasmic reticulum stress remodels alveolar bone formation after tooth extraction. J Cell Mol Med 24(21): 12411-12420, 2020. https://doi.org/10.1111/jcmm.15753.CrossRefPubMedPubMedCentral

24.

Chatterjee M, Faot F, Correa C, Duyck J, Naert I, Vandamme K: A robust methodology for the quantitative assessment of the rat jawbone microstructure. Int J Oral Sci 9(2): 87-94, 2017. https://doi.org/10.1038/ijos.2017.11.CrossRefPubMedPubMedCentral

25.

Wang JY, Huo L, Yu RQ, Rao NJ, Lu WW, Zheng LW: Skeletal site-specific response of jawbones and long bones to surgical interventions in rats treated with zoledronic acid. Biomed Res Int 2019: 5138175, 2019. https://doi.org/10.1155/2019/5138175.CrossRefPubMedPubMedCentral

26.

Bruker-MicroCT. Bruker Micro - CT Academy Bruker Micro-CT Academy. Bruker Micro-CT Acad 2:1–2, 2015.

27.

Otsu, N: A threshold selection method from gray-level histograms. IEEE Trans. Syst. Man Cybern 9(1): 62– 66, 1979. https://doi.org/10.1109/TSMC.1979.4310076.CrossRef

28.

Queiroz PM, Rovaris K, Santaella GM, Haiter-Neto F, Freitas DQ: Comparison of automatic and visual methods used for image segmentation in Endodontics: a microCT study. J Appl Oral Sci 25(6):674-79, 2017.CrossRefPubMedPubMedCentral

29.

van Vlijmen OJ, Rangel FA, Bergé SJ, Bronkhorst EM, Becking AG, Kuijpers-Jagtman AM: Measurements on 3D models of human skulls derived from two different cone beam CT scanners. Clin Oral Investig 15(5): 721-727, 2011. https://doi.org/10.1007/s00784-010-0440-8.CrossRefPubMed

30.

Ribeiro LL, Bosco AF, Nagata MJ, de Melo LG: Influence of bioactive glass and/or acellular dermal matrix on bone healing of surgically created defects in rat tibiae: a histological and histometric study. Int J Oral Maxillofac Implants 23(5): 811-817, 2008.PubMed

31.

Truedsson A, Wang JS, Lindberg P, Gordh M, Sunzel B, Warfvinge G: Bone substitute as an on-lay graft on rat tibia. Clin Oral Implants Res 21(4): 424-429, 2010. https://doi.org/10.1111/j.1600-0501.2009.01875.x.CrossRefPubMed

32.

Dias PC, Limirio PHJO, Linhares CRB, Bergamini ML, Rocha FS, Morais RB, Balbi APC, Hiraki KRN, Dechichi P: Hyperbaric Oxygen therapy effects on bone regeneration in Type 1 diabetes mellitus in rats. Connect Tissue Res 59(6): 574-580, 2018. https://doi.org/10.1080/03008207.2018.1434166.CrossRefPubMed

33.

Mendes EM, Irie MS, Rabelo GD, Borges JS, Dechichi P, Diniz RS, Soares PBF: Effects of ionizing radiation on woven bone: influence on the osteocyte lacunar network, collagen maturation, and microarchitecture. Clin Oral Investig 24(8): 2763-2771, 2020. https://doi.org/10.1007/s00784-019-03138-x.CrossRefPubMed

34.

Arioka M, Zhang X, Li Z, Tulu US, Liu Y, Wang L, Yuan X, Helms JA. Osteoporotic changes in the periodontium impair alveolar bone healing. J Dent Res 98(4): 450-458, 2019. https://doi.org/10.1177/0022034518818456.CrossRefPubMedPubMedCentral

35.

Miranda TS, Napimoga MH, De Franco L, Marins LM, Malta FS, Pontes LA, Morelli FM, Duarte PM: Strontium ranelate improves alveolar bone healing in estrogen-deficient rats. J Periodontol 91(11): 1465-1474, 2020. https://doi.org/10.1002/JPER.19-0561.CrossRefPubMed

36.

Vieira AE, Repeke CE, Ferreira Junior Sde B, Colavite PM, Biguetti CC, Oliveira RC, Assis GF, Taga R, Trombone AP, Garlet GP: Intramembranous bone healing process subsequent to tooth extraction in mice: micro-computed tomography, histomorphometric and molecular characterization. PLoS One 10(5): e0128021, 2015. https://doi.org/10.1371/journal.pone.0128021.CrossRefPubMedPubMedCentral

37.

Lazenby RA, Skinner MM, Kivell TL, Hublin JJ: Scaling VOI size in 3D μCT studies of trabecular bone: a test of the over-sampling hypothesis. Am J Phys Anthropol 144(2): 196-203, 2011. https://doi.org/10.1002/ajpa.21385.CrossRefPubMed

38.

Whitehouse WJ, Dyson ED: Scanning electron microscope studies of trabecular bone in the proximal end of the human femur. J Anat 118(Pt 3): 417-444, 1974.PubMedPubMedCentral

39.

Scala A, Lang NP, Schweikert MT, de Oliveira JA, Rangel-Garcia I Jr, Botticelli D: Sequential healing of open extraction sockets. An experimental study in monkeys. Clin Oral Implants Res 25(3): 288–295, 2014. https://doi.org/10.1111/clr.12148.

40.

Einhorn TA, Gerstenfeld LC: Fracture healing: mechanisms and interventions. Nat Rev Rheumatol 11(1): 45-54, 2015. https://doi.org/10.1038/nrrheum.2014.164.CrossRefPubMed

41.

Zhang H, Chavez MB, Kolli TN, Tan MH, Fong H, Chu EY, Li Y, Ren X, Watanabe K, Kim DG, Foster BL: Dentoalveolar defects in the hyp mouse model of x-linked hypophosphatemia. J Dent Res (4):419-428, 2020. https://doi.org/10.1177/0022034520901719.CrossRef

42.

Marmary Y, Brayer L, Tzukert A, Feller L: Alveolar bone repair following extraction of impacted mandibular third molars. Oral Surg Oral Med Oral Pathol 61(4): 324-326, 1986. https://doi.org/10.1016/0030-4220(86)90409-3.CrossRefPubMed

43.

Van der Weijden F, Dell'Acqua F, Slot DE: Alveolar bone dimensional changes of post-extraction sockets in humans: a systematic review. J Clin Periodontol 36(12): 1048-1058, 2009. https://doi.org/10.1111/j.1600-051X.2009.01482.x.CrossRefPubMed

44.

Bernabé PF, Melo LG, Cintra LT, Gomes-Filho JE, Dezan E Jr, Nagata MJ: Bone healing in critical-size defects treated with either bone graft, membrane, or a combination of both materials: a histological and histometric study in rat tibiae. Clin Oral Implants Res 23(3): 384-388, 2012. https://doi.org/10.1111/j.1600-0501.2011.02166.x.CrossRefPubMed

45.

de Freitas Silva L, de Carvalho Reis ENR, Barbara TA, Bonardi JP, Garcia IR Junior, de Carvalho PSP, Ponzoni D: Assessment of bone repair in critical-size defect in the calvarium of rats after the implantation of tricalcium phosphate beta (β-TCP). Acta Histochem 119(6): 624-631, 2017. https://doi.org/10.1016/j.acthis.2017.07.003.CrossRef

46.

Soares PBF, Soares CJ, Limirio PHJO, Lara VC, Moura CCG, Zanetta-Barbosa D: Biomechanical and morphological changes produced by ionizing radiation on bone tissue surrounding dental implant. J Appl Oral Sci 28: e20200191, 2020. https://doi.org/10.1590/1678-7757-2020-0191.CrossRefPubMedPubMedCentral

47.

Schmitz JP, Hollinger JO: The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin Orthop Relat Res (205):299-308, 1986.CrossRef

48.

Chin VK, Shinagawa A, Naclério-Homem Mda G: Bone healing of mandibular critical-size defects in spontaneously hypertensive rats. Braz Oral Res 27(5):423-430, 2013. https://doi.org/10.1590/S1806-83242013000500006.CrossRefPubMed

49.

Retzepi M, Donos N: Guided Bone Regeneration: biological principle and therapeutic applications. Clin Oral Implants Res 21(6):567-576, 2010. https://doi.org/10.1111/j.1600-0501.2010.01922.x.CrossRefPubMed

50.

Luvizuto ER, Dias SM, Queiroz TP, Okamoto T, Garcia IR Jr, Okamoto R, Dornelles RC: Osteocalcin immunolabeling during the alveolar healing process in ovariectomized rats treated with estrogen or raloxifene. Bone 46(4): 1021-1029, 2010. https://doi.org/10.1016/j.bone.2009.12.016.CrossRefPubMed

51.

Luvizuto ER, Queiroz TP, Dias SM, Okamoto T, Dornelles RC, Garcia IR Jr, Okamoto R: Histomorphometric analysis and immunolocalization of RANKL and OPG during the alveolar healing process in female ovariectomized rats treated with oestrogen or raloxifene. Arch Oral Biol 55(1): 52-59, 2010. https://doi.org/10.1016/j.archoralbio.2009.11.001.CrossRefPubMed

52.

Faot F, Chatterjee M, de Camargos GV, Duyck J, Vandamme K: Micro-CT analysis of the rodent jaw bone micro-architecture: A systematic review. Bone Rep 2: 14-24, 2015. https://doi.org/10.1016/j.bonr.2014.10.005.CrossRefPubMedPubMedCentral

53.

Irie MS, Spin-Neto R, Borges JS, Wenzel A, Soares PBF: Effect of data binning and frame averaging for micro-CT image acquisition on the morphometric outcome of bone repair assessment. Sci Rep 26;12(1):1424, 2022. https://doi.org/10.1038/s41598-022-05459-6.

54.

Feldkamp LA, Davis LC, Kress J: Practical cone-beam algorithm. J Opt Soc Am 1(6):612–19, 1984.CrossRef

55.

Clark DP, Badea CT: Micro-CT of rodents: state-of-the-art and future perspectives. Phys Med 30(6):619-34, 2014. https://doi.org/10.1016/j.ejmp.2014.05.011.CrossRefPubMedPubMedCentral

56.

Van Dessel J, Nicolielo LF, Huang Y, Coudyzer W, Salmon B, Lambrichts I, Jacobs R: Accuracy and reliability of different cone beam computed tomography (CBCT) devices for structural analysis of alveolar bone in comparison with multislice CT and micro-CT. Eur J Oral Implantol 10(1):95-105, 2017.PubMed

57.

Wang CX, Zeng L, Guo YM, Zhang LL: Wavelet tight frame and prior image-based image reconstruction from limited-angle projection data. Inverse Problems and Imaging 11(6): 917–948, 2017.CrossRef

58.

Wang CX, Zeng L. Error bounds and stability in the L0 regularized for CT reconstruction from small projections: Inverse Problems and Imaging 10(3): 829–853, 2016.

59.

Wu WW, Zhang YB, Wang Q, Liu FL, Chen PJ, Yu HY: Low-dose spectral CT reconstruction using image gradient ℓ0–norm and tensor dictionary. Applied Mathematical Modelling 63: 538–557, 2018.CrossRefPubMedPubMedCentral

60.

Yu HY, Wang G. Compressed sensing based interior tomography: Phys. Med. Biol 54(9): 2791–2805, 2009.CrossRef

61.

Bansal M, Kumar M, Sachdeva M, Mittal A: Transfer learning for image classification using VGG19: Caltech-101 image data set. J Ambient Intell Humaniz Comput 17:1-12, 2021. https://doi.org/10.1007/s12652-021-03488-z.CrossRef

62.

Kaur A, Kumar m, Jindal M.K: Shi-Tomasi corner detector for cattle identification from muzzle print image pattern. Ecol Informatics 68: 101549, 2022. https://doi.org/10.1016/j.ecoinf.2021.101549.

Title: Definition of the Region of Interest for the Assessment of Alveolar Bone Repair Using Micro-computed Tomography
Authors: Juliana Simeão Borges
Vitor Cardoso Costa
Milena Suemi Irie
Gabriella Lopes de Rezende Barbosa
Rubens Spin-Neto
Priscilla Barbosa Ferreira Soares
Publication date: 07-09-2022
Publisher: Springer International Publishing
Keywords: Tooth Extraction
Computed Tomography
Computed Tomography
Tooth Extraction
Published in: Journal of Imaging Informatics in Medicine / Issue 1/2023
Print ISSN: 2948-2925
Electronic ISSN: 2948-2933
DOI: https://doi.org/10.1007/s10278-022-00693-w

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Definition of the Region of Interest for the Assessment of Alveolar Bone Repair Using Micro-computed Tomography

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