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http://dx.doi.org/10.5624/isd.2020.50.3.199

In vivo quantification of mandibular bone remodeling and vascular changes in a Wistar rat model: A novel HR-MRI and micro-CT fusion technique  

Song, Dandan (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Shujaat, Sohaib (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Zhao, Ruiting (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Huang, Yan (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Shaheen, Eman (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Van Dessel, Jeroen (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Orhan, Kaan (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Velde, Greetje Vande (Biomedical MRI, Department of Imaging and Pathology, Faculty of Medicine)
Coropciuc, Ruxandra (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Pauwels, Ruben (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Politis, Constantinus (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Jacobs, Reinhilde (OMFS IMPATH Research Group, Department of Imaging and Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals Leuven)
Publication Information
Imaging Science in Dentistry / v.50, no.3, 2020 , pp. 199-208 More about this Journal
Abstract
Purpose: This study was performed to introduce an in vivo hybrid multimodality technique involving the coregistration of micro-computed tomography (micro-CT) and high-resolution magnetic resonance imaging (HR-MRI) to concomitantly visualize and quantify mineralization and vascularization at follow-up in a rat model. Materials and Methods: Three adult female rats were randomly assigned as test subjects, with 1 rat serving as a control subject. For 20 weeks, the test rats received a weekly intravenous injection of 30 ㎍/kg zoledronic acid, and the control rat was administered a similar dose of normal saline. Bilateral extraction of the lower first and second molars was performed after 10 weeks. All rats were scanned once every 4 weeks with both micro-CT and HR-MRI. Micro-CT and HR-MRI images were registered and fused in the same 3-dimensional region to quantify blood flow velocity and trabecular bone thickness at T0 (baseline), T4 (4 weeks), T8 (8 weeks), T12 (12 weeks), T16 (16 weeks), and T20 (20 weeks). Histological assessment was the gold standard with which the findings were compared. Results: The histomorphometric images at T20 aligned with the HR-MRI findings, with both test and control rats demonstrating reduced trabecular bone vasculature and blood vessel density. The micro-CT findings were also consistent with the histomorphometric changes, which revealed that the test rats had thicker trabecular bone and smaller marrow spaces than the control rat. Conclusion: The combination of micro-CT and HR-MRI may be considered a powerful non-invasive novel technique for the longitudinal quantification of localized mineralization and vascularization.
Keywords
Vascular Remodeling; Radiology; Jaw; Rats;
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1 Maes C. Role and regulation of vascularization processes in endochondral bones. Calcif Tissue Int 2013; 92: 307-23.   DOI
2 Driessens M. Circulatory aspects of reflex sympathetic dystrophy. In: Schoutens A, Gardeniers JW, Hughes SP. Bone circulation and vascularization in normal and pathological conditions. New York: Springer; 1993. p. 217-31.
3 Boerckel JD, Uhrig BA, Willett NJ, Huebsch N, Guldberg RE. Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc Natl Acad Sci U S A 2011; 108: E674-80.   DOI
4 Eghbali-Fatourechi GZ, Modder UI, Charatcharoenwitthaya N, Sanyal A, Undale AH, Clowes JA, et al. Characterization of circulating osteoblast lineage cells in humans. Bone 2007; 40: 1370-7.   DOI
5 Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J, et al. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 2009; 458: 524-8.   DOI
6 Thompson B, Towler DA. Arterial calcification and bone physiology: role of the bone-vascular axis. Nat Rev Endocrinol 2012; 8: 529-43.   DOI
7 Mark H, Penington A, Nannmark U, Morrison W, Messina A. Microvascular invasion during endochondral ossification in experimental fractures in rats. Bone 2004; 35: 535-42.   DOI
8 Deshpande SS, Donneys A, Farberg AS, Tchanque-Fossuo CN, Felice PA, Buchman SR. Quantification and characterization of radiation-induced changes to mandibular vascularity using micro-computed tomography. Ann Plast Surg 2014; 72: 100-3.   DOI
9 Prajapati SI, Keller C. Contrast enhanced vessel imaging using microCT. J Vis Exp 2011; 47: 2377.
10 Abma E, Stock E, De Spiegelaere W, Van Brantegem L, Vanderperren K, Ni Y, et al. Power Doppler ultrasound and contrast- enhanced ultrasound demonstrate non-invasive tumour vascular response to anti-vascular therapy in canine cancer patients. Sci Rep 2019; 9: 9262.   DOI
11 Hillier ML, Bell LS. Differentiating human bone from animal bone: a review of histological methods. J Forensic Sci 2007; 52: 249-63.   DOI
12 Jorgensen SM, Demirkaya O, Ritman EL. Three-dimensional imaging of vasculature and parenchyma in intact rodent organs with X-ray micro-CT. Am J Physiol 1998; 275: H1103-14.
13 Yang J, Pham SM, Crabbe DL. High-resolution micro-CT evaluation of mid-to long-term effects of estrogen deficiency on rat trabecular bone. Acad Radiol 2003; 10: 1153-8.   DOI
14 Fei J, Peyrin F, Malaval L, Vico L, Lafage-Proust MH. Imaging and quantitative assessment of long bone vascularization in the adult rat using microcomputed tomography. Anat Rec (Hoboken) 2010; 293: 215-24.   DOI
15 Roche B, David V, Vanden-Bossche A, Peyrin F, Malaval L, Vico L, et al. Structure and quantification of microvascularisation within mouse long bones: what and how should we measure? Bone 2012; 50: 390-9.   DOI
16 Weinstein RS, Wan C, Liu Q, Wang Y, Almeida M, O'Brien CA, et al. Endogenous glucocorticoids decrease skeletal angiogenesis, vascularity, hydration, and strength in aged mice. Aging Cell 2010; 9: 147-61.   DOI
17 Ding WG, Wei ZX, Liu JB. Reduced local blood supply to the tibial metaphysis is associated with ovariectomy-induced osteoporosis in mice. Connect Tissue Res 2011; 52: 25-9.   DOI
18 Barentsz JO, Engelbrecht M, Jager GJ, Witjes JA, de LaRosette J, van der Sanden BP, et al. Fast dynamic gadolinium-enhanced MR imaging of urinary bladder and prostate cancer. J Magn Reson Imaging 1999; 10: 295-304.   DOI
19 Zagorchev L, Oses P, Zhuang ZW, Moodie K, Mulligan-Kehoe MJ, Simons M, et al. Micro computed tomography for vascular exploration. J Angiogenes Res 2010; 2: 7.   DOI
20 Benjaminsen IC, Graff BA, Brurberg KG, Rofstad EK. Assessment of tumor blood perfusion by high-resolution dynamic contrast-enhanced MRI: a preclinical study of human melanoma xenografts. Magn Reson Med 2004; 52: 269-76.   DOI
21 Liang H, Yang Y, Yang K, Wu Y, Boone JM, Cherry SR. A microPET/CT system for in vivo small animal imaging. Phys Med Biol 2007; 52: 3881-94.   DOI
22 Bernsen MR, Vaissier PE, Van Holen R, Booij J, Beekman FJ, de Jong M. The role of preclinical SPECT in oncological and neurological research in combination with either CT or MRI. Eur J Nucl Med Mol Imaging 2014; 41 Suppl 1: S36-49.
23 Klodowski K, Kaminski J, Nowicka K, Tarasiuk J, Wronski S, Swietek M, et al. Micro-imaging of implanted scaffolds using combined MRI and micro-CT. Comput Med Imaging Graph 2014; 38: 458-68.   DOI
24 Basha MA, AlAzzazy MZ, Ahmed AF, Yousef HY, Shehata SM, El Sammak DA, et al. Does a combined CT and MRI protocol enhance the diagnostic efficacy of LI-RADS in the categorization of hepatic observations? A prospective comparative study. Eur Radiol 2018; 28: 2592-603.   DOI
25 Lin MT, Wang CC, Cheng YF, Eng HL, Yen YH, Tsai MC, et al. Comprehensive comparison of multiple-detector computed tomography and dynamic magnetic resonance imaging in the diagnosis of hepatocellular carcinoma with varying degrees of fibrosis. PLoS One 2016; 11: e0166157.   DOI
26 Huang TC, Chang CK, Liao CH, Ho YJ. Quantification of blood flow in internal cerebral artery by optical flow method on digital subtraction angiography in comparison with timeof-flight magnetic resonance angiography. PLoS One 2013; 8: e54678.   DOI
27 Badea CT, Hedlund LW, De Lin M, Boslego Mackel JF, Johnson GA. Tumor imaging in small animals with a combined micro-CT/micro-DSA system using iodinated conventional and blood pool contrast agents. Contrast Media Mol Imaging 2006; 1: 153-64.   DOI
28 Longo AB, Sacco SM, Ward WE. Proper positioning and restraint of a rat hind limb for focused high resolution imaging of bone micro-architecture using in vivo micro-computed tomography. J Vis Exp 2017; 129: 56346.
29 Soares MQ, Van Dessel J, Jacobs R, da Silva Santos PS, Cestari TM, Garlet GP, et al. Zoledronic acid induces site-specific structural changes and decreases vascular area in the alveolar bone. J Oral Maxillofac Surg 2018; 76: 1893-901.   DOI
30 Sharma D, Hamlet S, Petcu E, Ivanovski S. Animal models for bisphosphonate-related-osteonecrosis of the jaws - an appraisal. Oral Dis 2013; 19: 747-54.   DOI
31 Faot F, Chatterjee M, de Camargos G, Duyck J, Vandamme K. Micro-CT analysis of the rodent jaw bone micro-architecture: a systematic review. Bone Rep 2015; 2: 14-24.   DOI
32 Siddiqui JA, Partridge NC. Physiological bone remodeling: systemic regulation and growth factor involvement. Physiology (Bethesda) 2016; 31: 233-45.
33 Bamias A, Kastritis E, Bamia C, Moulopoulos LA, Melakopoulos I, Bozas G. Osteonecrosis of the jaw in cancer after treatment with bisphosphonates: incidence and risk factors. J Clin Oncol 2005; 23: 8580-7.   DOI
34 Principi M, Italiani M, Guiducci A, Aprile I, Muti M, Giulianelli G, et al. Perfusion MRI in the evaluation of the relationship between tumour growth, necrosis and angiogenesis in glioblastomas and grade 1 meningiomas. Neuroradiology 2003; 45: 205-11.   DOI
35 Law M, Cha S, Knopp EA, Johnson G, Arnett J, Litt AW. High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. Radiology 2002; 222: 715-21.   DOI
36 Kress B, Gottschalk A, Anders L, Stippich C, Palm F, Bahren W, et al. High-resolution dental magnetic resonance imaging of inferior alveolar nerve responses to the extraction of third molars. Eur Radiol 2004; 14: 1416-20.   DOI
37 Lee SJ, Kim JH, Kim YM, Lee GK, Lee EJ, Park IS, et al. Perfusion MR imaging in gliomas: comparison with histologic tumor grade. Korean J Radiol 2001; 2: 1-7.   DOI
38 Vandersteen M, Beuls E, Gelan J, Adriaensens P, Vanormelingen L, Palmers Y, et al. High field magnetic resonance imaging of normal and pathologic human medulla oblongata. Anat Rec 1994; 238: 277-86.   DOI
39 Jacobs R, Lambrichts I, Liang X, Martens W, Mraiwa N, Adriaensens P, et al. Neurovascularization of the anterior jaw bones revisited using high-resolution magnetic resonance imaging. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007; 103: 683-93.   DOI
40 Du Tolt DF, Nortje C. The maxillae: integrated and applied anatomy relevant to dentistry. SADJ 2003; 58: 325-30.
41 Batiste DL, Kirkley A, Laverty S, Thain LM, Spouge AR, Gati JS, et al. High-resolution MRI and micro-CT in an ex vivo rabbit anterior cruciate ligament transection model of osteoarthritis. Osteoarthritis Cartilage 2004; 12: 614-26.   DOI
42 Kun-Darbois JD, Libouban H, Mabilleau G, Pascaretti-Grizon F, Chappard D. Bone mineralization and vascularization in bisphosphonate- related osteonecrosis of the jaw: an experimental study in the rat. Clin Oral Investig 2018; 22: 2997-3006.   DOI
43 Bi Y, Gao Y, Ehirchiou D, Cao C, Kikuiri T, Le A, et al. Bisphosphonates cause osteonecrosis of the jaw-like disease in mice. Am J Pathol 2010; 177: 280-90.   DOI