{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:48:23Z","timestamp":1787028503650,"version":"build-2736575974"},"reference-count":40,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T00:00:00Z","timestamp":1678060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Currently, computed tomography and conventional X-ray radiography usually generate a micro-artifact around metal implants. This metal artifact frequently causes false positive or negative diagnoses of bone maturation or pathological peri-implantitis around implants. In an attempt to repair the artifacts, a highly specific nanoprobe, an osteogenic biomarker, and nano-Au-Pamidronate were designed to monitor the osteogenesis. In total, 12 Sprague Dawley rats were included in the study and could be chategorized in 3 groups: 4 rats in the X-ray and CT group, 4 rats in the NIRF group, and 4 rats in the sham group. A titanium alloy screw was implanted in the anterior hard palate. The X-ray, CT, and NIRF images were taken 28 days after implantation. The X-ray showed that the tissue surrounded the implant tightly; however, a gap of metal artifacts was noted around the interface between dental implants and palatal bone. Compared to the CT image, a fluorescence image was noted around the implant site in the NIRF group. Furthermore, the histological implant-bone tissue also exhibited a significant NIRF signal. In conclusion, this novel NIRF molecular imaging system precisely identifies the image loss caused by metal artifacts and can be applied to monitoring bone maturation around orthopedic implants. In addition, by observing the new bone formation, a new principle and timetable for an implant osseointegrated with bone can be established and a new type of implant fixture or surface treatment can be evaluated using this system.<\/jats:p>","DOI":"10.3390\/ijms24055032","type":"journal-article","created":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T04:29:58Z","timestamp":1678076998000},"page":"5032","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["A Non-Invasive Method for Monitoring Osteogenesis and Osseointegration Using Near-Infrared Fluorescent Imaging: A Model of Maxilla Implantation in Rats"],"prefix":"10.3390","volume":"24","author":[{"given":"Chien-Chou","family":"Lin","sequence":"first","affiliation":[{"name":"Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei 110, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li-Hsuan","family":"Chiu","sequence":"additional","affiliation":[{"name":"McLean Imaging Center, McLean Hospital and Harvard Medical School, Belmont, MA 02478, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walter H.","family":"Chang","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Chung Yuan Christian University, Taoyuan 320, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng-An J.","family":"Lin","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Chung Yuan Christian University, Taoyuan 320, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5728-0571","authenticated-orcid":false,"given":"Ruei-Ming","family":"Chen","sequence":"additional","affiliation":[{"name":"Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei 110, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3649-6680","authenticated-orcid":false,"given":"Yuan-Soon","family":"Ho","sequence":"additional","affiliation":[{"name":"Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei 110, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chun S.","family":"Zuo","sequence":"additional","affiliation":[{"name":"McLean Imaging Center, McLean Hospital and Harvard Medical School, Belmont, MA 02478, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Austin","family":"Changou","sequence":"additional","affiliation":[{"name":"Ph.D. Program for Translational Medicine, College of Medicine and Technology, Taipei Medical University, Taipei 110, Taiwan"},{"name":"Core Facility Center, Office of Research and Development, Taipei Medical University, Taipei 110, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yue-Fa","family":"Cheng","sequence":"additional","affiliation":[{"name":"College of Basic Medicine, North China University of Science and Technology, Tangshan 066008, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Fu T.","family":"Lai","sequence":"additional","affiliation":[{"name":"McLean Imaging Center, McLean Hospital and Harvard Medical School, Belmont, MA 02478, USA"},{"name":"Institute of Graduate Clinical Medicine, Taipei Medical University, Taipei 110, Taiwan"},{"name":"Department of Research and Department of Dentistry, Taipei Medical University-Shuang-Ho Hospital, New Taipei City 235, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1111\/clr.12048","article-title":"In vitro assessment of artifacts induced by titanium dental implants in cone beam computed tomography","volume":"24","author":"Benic","year":"2013","journal-title":"Clin. Oral Implants Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1080\/02841850410001402","article-title":"Low-dose dental computed tomography: Significant dose reduction without loss of image quality","volume":"45","author":"Rustemeyer","year":"2004","journal-title":"Acta Radiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1148\/radiology.164.2.3602406","article-title":"Reduction of CT artifacts caused by metallic implants","volume":"164","author":"Kalender","year":"1987","journal-title":"Radiology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1109\/42.897816","article-title":"X-ray CT metal artifact reduction using wavelets: An application for imaging total hip prostheses","volume":"19","author":"Zhao","year":"2000","journal-title":"IEEE Trans. Med. Imaging"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1259\/dmfr\/32579161","article-title":"Beam hardening artefacts occur in dental implant scans with the NewTom cone beam CT but not with the dental 4-row multidetector CT","volume":"36","author":"Draenert","year":"2007","journal-title":"Dentomaxillofac. Radiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1111\/j.1600-0501.2009.01905.x","article-title":"Accuracy of measuring the cortical bone thickness adjacent to dental implants using cone beam computed tomography","volume":"21","author":"Razavi","year":"2010","journal-title":"Clin. Oral Implants Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1111\/j.1600-0501.2009.01817.x","article-title":"On cone-beam computed tomography artifacts induced by titanium implants","volume":"21","author":"Schulze","year":"2010","journal-title":"Clin. Oral Implants Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1007\/s13770-019-00208-9","article-title":"Near-Infrared Contrast Agents for Bone-Targeted Imaging","volume":"16","author":"Jung","year":"2019","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"120267","DOI":"10.1016\/j.biomaterials.2020.120267","article-title":"NIR fluorescence for monitoring in vivo scaffold degradation along with stem cell tracking in bone tissue engineering","volume":"258","author":"Kim","year":"2020","journal-title":"Biomaterials"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"153","DOI":"10.3109\/03008207.2015.1012586","article-title":"Near infrared fluorescence imaging for early detection, monitoring and improved intervention of diseases involving the joint","volume":"56","author":"Slooter","year":"2015","journal-title":"Connect. Tissue Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e1901224","DOI":"10.1002\/adhm.201901224","article-title":"Specific Small-Molecule NIR-II Fluorescence Imaging of Osteosarcoma and Lung Metastasis","volume":"9","author":"Zhou","year":"2020","journal-title":"Adv. Healthc. Mater."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2580","DOI":"10.1038\/s41598-020-59522-1","article-title":"Two new, near-infrared, fluorescent probes as potential tools for imaging bone repair","volume":"10","author":"Lin","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1146\/annurev.bioeng.8.061505.095721","article-title":"Biomechanical and molecular regulation of bone remodeling","volume":"8","author":"Robling","year":"2006","journal-title":"Annu. Rev. Biomed. Eng."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2496","DOI":"10.1021\/bc2003132","article-title":"Enhanced affinity bifunctional bisphosphonates for targeted delivery of therapeutic agents to bone","volume":"22","author":"Yewle","year":"2011","journal-title":"Bioconjug. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7969","DOI":"10.1002\/anie.200701216","article-title":"Synthesis of conjugatable bisphosphonates for molecular imaging of large animals","volume":"46","author":"Bhushan","year":"2007","journal-title":"Angew. Chem. Int. Ed."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1016\/j.bone.2012.07.020","article-title":"The effect of alendronate doped calcium phosphates on bone cells activity","volume":"51","author":"Boanini","year":"2012","journal-title":"Bone"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"19509","DOI":"10.1038\/s41598-022-24160-2","article-title":"Osteogenic differentiation and proliferation potentials of human bone marrow and umbilical cord-derived mesenchymal stem cells on the 3D-printed hydroxyapatite scaffolds","volume":"12","author":"Meesuk","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1038\/nbt1201-1148","article-title":"In vivo near-infrared fluorescence imaging of osteoblastic activity","volume":"19","author":"Zaheer","year":"2001","journal-title":"Nat. Biotechnol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e2101586","DOI":"10.1002\/adhm.202101586","article-title":"Unraveling an Innate Mechanism of Pathological Mineralization-Regulated Inflammation by a Nanobiomimetic System","volume":"10","author":"Wang","year":"2021","journal-title":"Adv. Healthc. Mater."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"6449","DOI":"10.1039\/C9TB01918A","article-title":"Hydroxyapatite-binding micelles for the detection of vascular calcification in atherosclerosis","volume":"7","author":"Chin","year":"2019","journal-title":"J. Mater. Chem. B"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Song, M.K., Park, S.I., and Cho, S.W. (2023). Circulating biomarkers for diagnosis and therapeutic monitoring in bone metastasis. J. Bone Miner. Metab., 1\u20138.","DOI":"10.1007\/s00774-022-01396-6"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1016\/j.cbpa.2003.08.007","article-title":"In vivo near-infrared fluorescence imaging","volume":"7","author":"Frangioni","year":"2003","journal-title":"Curr. Opin. Chem. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.1038\/2061328a0","article-title":"Fluorescence of bone","volume":"206","author":"Bachman","year":"1965","journal-title":"Nature"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/j.1749-6632.1998.tb08185.x","article-title":"Near-infrared images using continuous, phase-modulated, and pulsed light with quantitation of blood and blood oxygenation","volume":"838","author":"Chance","year":"1998","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1136\/jcp.20.5.717","article-title":"Autofluorescence of bone tissues","volume":"20","author":"Prentice","year":"1967","journal-title":"J. Clin. Pathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.cis.2006.05.026","article-title":"Nanoparticles for bioimaging","volume":"123","author":"Sharma","year":"2006","journal-title":"Adv. Colloid Interface Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1002\/jbm.a.33165","article-title":"Binding affinity of surface functionalized gold nanoparticles to hydroxyapatite","volume":"99","author":"Ross","year":"2011","journal-title":"J. Biomed. Mater. Res. A"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1039\/b9nr00317g","article-title":"Preparation of functionalized gold nanoparticles as a targeted X-ray contrast agent for damaged bone tissue","volume":"2","author":"Zhang","year":"2010","journal-title":"Nanoscale"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1002\/jbm.a.30923","article-title":"Increased osteoblast adhesion on nanograined hydroxyapatite and tricalcium phosphate containing calcium titanate","volume":"80","author":"Ergun","year":"2007","journal-title":"J. Biomed. Mater. Res. A"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1002\/jbm.a.32454","article-title":"Effects of the nanostructure and nanoporosity on bioactive nanohydroxyapatite\/reconstituted collagen by electrodeposition","volume":"92","author":"Ou","year":"2010","journal-title":"J. Biomed. Mater. Res. A"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1021\/am201311c","article-title":"Biocompatible magnetite\/gold nanohybrid contrast agents via green chemistry for MRI and CT bioimaging","volume":"4","author":"Narayanan","year":"2012","journal-title":"ACS Appl. Mater. Interfaces"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1118\/1.4939062","article-title":"A nanocomposite of Au-AgI core\/shell dimer as a dual-modality contrast agent for X-ray computed tomography and photoacoustic imaging","volume":"43","author":"Orza","year":"2016","journal-title":"Med. Phys."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1021\/nn800632j","article-title":"Synthesis, characterization, and bioconjugation of fluorescent gold nanoclusters toward biological labeling applications","volume":"3","author":"Lin","year":"2009","journal-title":"ACS Nano"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"309","DOI":"10.7150\/ntno.47734","article-title":"Pulmonary fate and consequences of transferrin-functionalized gold nanoparticles","volume":"5","author":"Konduru","year":"2021","journal-title":"Nanotheranostics"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.joca.2003.11.005","article-title":"Early diagnosis of osteoarthritis using cathepsin B sensitive near-infrared fluorescent probes","volume":"12","author":"Lai","year":"2004","journal-title":"Osteoarthr. Cartil."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4337","DOI":"10.1021\/nn102752a","article-title":"Fluorescent gold nanoclusters as a biocompatible marker for in vitro and in vivo tracking of endothelial cells","volume":"5","author":"Wang","year":"2011","journal-title":"ACS Nano"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"5111","DOI":"10.1021\/nn300768d","article-title":"Rapid transformation of protein-caged nanomaterials into microbubbles as bimodal imaging agents","volume":"6","author":"Lin","year":"2012","journal-title":"ACS Nano"},{"key":"ref_38","unstructured":"Chiu, L., Kung, F., Yang, M., Tsai, Y., Chang, W., and Lai, W.-F. (2013, January 12\u201316). A Novel Near Infra-Red Fluorescent Probes to Repair Metal Artifact After Implantation. Proceedings of the Technical Proceedings of the 2013 NSTI Nanotechnology Conference and Expo, NSTI-Nanotech 2013, Washington, DC, USA."},{"key":"ref_39","unstructured":"Yeh, S., Chiu, L., Lin, C., Wan, R., Chang, W., and Lai, W.-F. (2012, January 2\u20134). Early Detection of Prostate Cancers and Their Bone Metastasis using Near-Infrared Fluorescent Imaging. Proceedings of the 3rd International NanoMedicine Conference, Sydney, Australia."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wang, K.H., Wang, Y.M., Chiu, L.H., Chen, T.C., Tsai, Y.H., Zuo, C.S., Chen, K.C., Changou, C.A., and Lai, W.T. (2018). Optical imaging of ovarian cancer using a matrix metalloproteinase-3-sensitive near-infrared fluorescent probe. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0202610"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/5032\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:48:50Z","timestamp":1760122130000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/5032"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,6]]},"references-count":40,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["ijms24055032"],"URL":"https:\/\/doi.org\/10.3390\/ijms24055032","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,6]]}}}