Evaluation of the first maxillary molar post-extraction socket as a model for dental implant osseointegration research
Zhibin Du
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Search for more papers by this authorRyan S. B. Lee
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Search for more papers by this authorStephen Hamlet
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Search for more papers by this authorNghiem Doan
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Search for more papers by this authorCorresponding Author
Saso Ivanovski
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Corresponding authors:
Professor Yin Xiao
Institute of Health and Biomedical Innovation
Queensland University of Technology
Kelvin Grove Campus
Brisbane
Qld 4059
Australia
Tel.: +61 7 31386240
Fax: +61 7 31386030
e-mail: [email protected]
and
Professor Saso Ivanovski
Griffith University
Gold Coast Campus
Griffith Centre, G40_7.81
Parkland Drive
Southport
QLD 4222
Australia
Tel.: +61 7 56780741
Fax: +61 7 56780708
e-mail: [email protected]
Search for more papers by this authorCorresponding Author
Yin Xiao
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Corresponding authors:
Professor Yin Xiao
Institute of Health and Biomedical Innovation
Queensland University of Technology
Kelvin Grove Campus
Brisbane
Qld 4059
Australia
Tel.: +61 7 31386240
Fax: +61 7 31386030
e-mail: [email protected]
and
Professor Saso Ivanovski
Griffith University
Gold Coast Campus
Griffith Centre, G40_7.81
Parkland Drive
Southport
QLD 4222
Australia
Tel.: +61 7 56780741
Fax: +61 7 56780708
e-mail: [email protected]
Search for more papers by this authorZhibin Du
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Search for more papers by this authorRyan S. B. Lee
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Search for more papers by this authorStephen Hamlet
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Search for more papers by this authorNghiem Doan
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Search for more papers by this authorCorresponding Author
Saso Ivanovski
School of Dentistry and Oral Health, Griffith University, Southport, Qld, Australia
Corresponding authors:
Professor Yin Xiao
Institute of Health and Biomedical Innovation
Queensland University of Technology
Kelvin Grove Campus
Brisbane
Qld 4059
Australia
Tel.: +61 7 31386240
Fax: +61 7 31386030
e-mail: [email protected]
and
Professor Saso Ivanovski
Griffith University
Gold Coast Campus
Griffith Centre, G40_7.81
Parkland Drive
Southport
QLD 4222
Australia
Tel.: +61 7 56780741
Fax: +61 7 56780708
e-mail: [email protected]
Search for more papers by this authorCorresponding Author
Yin Xiao
Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, Qld, Australia
Corresponding authors:
Professor Yin Xiao
Institute of Health and Biomedical Innovation
Queensland University of Technology
Kelvin Grove Campus
Brisbane
Qld 4059
Australia
Tel.: +61 7 31386240
Fax: +61 7 31386030
e-mail: [email protected]
and
Professor Saso Ivanovski
Griffith University
Gold Coast Campus
Griffith Centre, G40_7.81
Parkland Drive
Southport
QLD 4222
Australia
Tel.: +61 7 56780741
Fax: +61 7 56780708
e-mail: [email protected]
Search for more papers by this authorAbstract
Objectives
Published information regarding the use of rat jawbones for dental implant osseointegration research is limited and often inconsistent. This study assessed the suitability and feasibility of placing dental implants into the rat maxilla and to establish parameters to be used for dental implant research using this model.
Materials and methods
Forty-two customized titanium implants (2 × 3 mm) were placed bilaterally in the maxillary first molar area of 21 Sprague–Dawley rats. Every animal received two implants. The animals were subsequently sacrificed at days 3, 7, 14, 28 and 56 post-surgery. Resin-embedded sections of the implant and surrounding maxilla were prepared for histological and histomorphometric analyses.
Results
The mesial root of the first molar in the rat maxilla was the optimal site to place the implant. Although the most apical 2–3 threads of the implant penetrated into the sinus cavity, 2 mm of the remaining implant was embedded in the bone. New bone formation at day 7 around the implant increased further at day 14, as measured by the percentage of bone-to-implant contact (%BIC) and new bone area (%BA) in the implant thread chambers (55.1 ± 8.9% and 63.7 ± 7.7%, respectively). There was a further significant increase between day 14 and 28 (P < 0.05), however, no significant differences were found between day 28 and 56 in either %BIC or %BA.
Conclusions
The mesial root socket of the first molar in the rat maxilla is a useful model for dental implant research. Osseointegration following implant placement as measured by BIC plateaued after 28 days. The recommended implant dimensions are 1.5 mm in diameter and 2 mm in length.
References
- Abtahi, J., Agholme, F., Sandberg, O. & Aspenberg, P. (2013) Effect of local vs. systemic bisphosphonate delivery on dental implant fixation in a model of osteonecrosis of the jaw. Journal of Dental Research 92: 279–283.
- Abuhussein, H., Pagni, G., Rebaudi, A. & Wang, H.L. (2010) The effect of thread pattern upon implant osseointegration. Clinical Oral Implants Research 21: 129–136.
- Aerssens, J., Boonen, S., Lowet, G. & Dequeker, J. (1998) Interspecies differences in bone composition, density, and quality: potential implications for in vivo bone research. Endocrinology 139: 663–670.
- Aghaloo, T.L., Kang, B., Sung, E.C., Shoff, M., Ronconi, M., Gotcher, J.E., Bezouglaia, O., Dry, S.M. & Tetradis, S. (2011) Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. Journal of Bone and Mineral Research 26: 1871–1882.
- Albrektsson, T., Hansson, H. & Ivarsson, B. (1985) Interface analysis of titanium and zirconium bone implants. Biomaterials 6: 97–101.
- Anderson, M.L., Dhert, W.J., de Bruijn, J.D., Dalmeijer, R.A., Leenders, H., van Blitterswijk, C.A. & Verbout, A.J. (1999) Critical size defect in the goat's os ilium. A model to evaluate bone grafts and substitutes. Clinical Orthopaedics and Related Research 364: 231–239.
- Anitua, E.A. (2006) Enhancement of osseointegration by generating a dynamic implant surface. The Journal of Oral Implantology 32: 72–76.
- Baron, R., Tross, R. & Vignery, A. (1984) Evidence of sequential remodeling in rat trabecular bone: morphology, dynamic histomorphometry, and changes during skeletal maturation. The Anatomical record 208: 137–145.
- Berglundh, T. & Stavropoulos, A. (2012) Preclinical in vivo research in implant dentistry. Consensus of the eighth European workshop on periodontology. Journal of Clinical Periodontology 39(Suppl. 12): 1–5.
- Bierbaum, S., Hintze, V. & Scharnweber, D. (2012) Functionalization of biomaterial surfaces using artificial extracellular matrices. Biomatter 2: 132–141.
- den Boer, F.C., Patka, P., Bakker, F.C., Wippermann, B.W., van Lingen, A., Vink, G.Q., Boshuizen, K. & Haarman, H.J. (1999) New segmental long bone defect model in sheep: quantitative analysis of healing with dual energy X-ray absorptiometry. Journal of Orthopaedic Research 17: 654–660.
- Brunski, J.B. (1999) In vivo bone response to biomechanical loading at the bone/dental-implant interface. Advances in Dental Research 13: 99–119.
- Buchter, A., Joos, U., Wiesmann, H.P., Seper, L. & Meyer, U. (2006) Biological and biomechanical evaluation of interface reaction at conical screw-type implants. Head & Face Medicine 2: 5.
- Chai, Y. & Maxson, R.E., Jr. (2006) Recent advances in craniofacial morphogenesis. Developmental Dynamics 235: 2353–2375.
- Chang, P.C., Seol, Y.J., Cirelli, J.A., Pellegrini, G., Jin, Q., Franco, L.M., Goldstein, S.A., Chandler, L.A., Sosnowski, B. & Giannobile, W.V. (2010) PDGF-B gene therapy accelerates bone engineering and oral implant osseointegration. Gene Therapy 17: 95–104.
- Danz, J.C., Dalstra, M., Bosshardt, D.D., Katsaros, C. & Stavropoulos, A. (2013) A rat model for orthodontic translational expansive tooth movement. Orthodontics & Craniofacial Research 16: 223–233.
- Dominguez-Malagon, H.R., Gonzalez-Conde, E., Cano-Valdez, A.M., Luna-Ortiz, K. & Mosqueda-Taylor, A. (2014) Expression of hormonal receptors in osteosarcomas of the jaw bones: clinico-pathological analysis of 21 cases. Medicina Oral, Patología Oral y Cirugía Bucal 19: e44–e48.
- Donath, K. & Breuner, G. (1982) A method for the study of undecalcified bones and teeth with attached soft tissues*. Journal of Oral Pathology & Medicine 11: 318–326.
- Du, Z., Chen, J., Yan, F., Doan, N., Ivanovski, S. & Xiao, Y. (2013) Serum bone formation marker correlation with improved osseointegration in osteoporotic rats treated with simvastatin. Clinical Oral Implants Research 24: 422–427.
- Du, Z.B., Chen, J., Yan, F.H. & Xiao, Y. (2009) Effects of simvastatin on bone healing around titanium implants in osteoporotic rats. Clinical Oral Implants Research 20: 145–150.
- Froum, S.J., Simon, H., Cho, S.C., Elian, N., Rohrer, M.D. & Tarnow, D.P. (2005) Histologic evaluation of bone-implant contact of immediately loaded transitional implants after 6 to 27 months. The International Journal of Oral & Maxillofacial Implants 20: 54–60.
- Fujii, N., Kusakari, H. & Maeda, T. (1998) A histological study on tissue responses to titanium implantation in rat maxilla: the process of epithelial regeneration and bone reaction. Journal of Periodontology 69: 485–495.
- Fujii, N., Ohnishi, H., Shirakura, M., Nomura, S., Ohshima, H. & Maeda, T. (2003) Regeneration of nerve fibres in the peri-implant epithelium incident to implantation in the rat maxilla as demonstrated by immunocytochemistry for protein gene product 9.5 (PGP9.5) and calcitonin gene-related peptide (CGRP). Clinical Oral Implants Research 14: 240–247.
- Futami, T., Fujii, N., Ohnishi, H., Taguchi, N., Kusakari, H., Ohshima, H. & Maeda, T. (2000) Tissue response to titanium implants in the rat maxilla: ultrastructural and histochemical observations of the bone-titanium interface. Journal of Periodontology 71: 287–298.
- Giro, G., Coelho, P.G., Sales-Pessoa, R., Pereira, R.M., Kawai, T. & Orrico, S.R. (2011) Influence of estrogen deficiency on bone around osseointegrated dental implants: an experimental study in the rat jaw model. Journal of Oral and Maxillofacial Surgery 69: 1911–1918.
- Haga, M., Fujii, N., Nozawa-Inoue, K., Nomura, S., Oda, K., Uoshima, K. & Maeda, T. (2009) Detailed process of bone remodeling after achievement of osseointegration in a rat implantation model. The Anatomical Record (Hoboken) 292: 38–47.
- Helms, J.A. & Schneider, R.A. (2003) Cranial skeletal biology. Nature 423: 326–331.
- Hou, X., Weiler, M.A., Winger, J.N., Morris, J.R. & Borke, J.L. (2009) Rat model for studying tissue changes induced by the mechanical environment surrounding loaded titanium implants. The International Journal of Oral & Maxillofacial Implants 24: 800–807.
- Ikeda, H., Shiraiwa, M., Yamaza, T., Yoshinari, M., Kido, M.A., Ayukawa, Y., Inoue, T., Koyano, K. & Tanaka, T. (2002) Difference in penetration of horseradish peroxidase tracer as a foreign substance into the peri-implant or junctional epithelium of rat gingivae. Clinical Oral Implants Research 13: 243–251.
- Ikeda, H., Yamaza, T., Yoshinari, M., Ohsaki, Y., Ayukawa, Y., Kido, M.A., Inoue, T., Shimono, M., Koyano, K. & Tanaka, T. (2000) Ultrastructural and immunoelectron microscopic studies of the peri-implant epithelium-implant (Ti-6Al-4V) interface of rat maxilla. Journal of Periodontology 71: 961–973.
- Inouye, K.A., Bisch, F.C., Elsalanty, M.E., Zakhary, I., Khashaba, R.M. & Borke, J.L. (2014) Effect of metformin on periimplant wound healing in a rat model of type 2 diabetes. Implant Dentistry 23: 319–327.
- Javed, F. & Romanos, G.E. (2009) Impact of diabetes mellitus and glycemic control on the osseointegration of dental implants: a systematic literature review. Journal of Periodontology 80: 1719–1730.
- Karimbux, N.Y., Sirakian, A., Weber, H.P. & Nishimura, I. (1995) A new animal model for molecular biological analysis of the implant-tissue interface: spatial expression of type XII collagen mRNA around a titanium oral implant. The Journal of Oral Implantology 21: 107–113; discussion 114–105.
- Kavanagh, P., Gould, T.R., Brunette, D.M. & Weston, L. (1985) A rodent model for the investigation of dental implants. The Journal of Prosthetic Dentistry 54: 252–257.
- Kim, D.-G., Huja, S.S., Tee, B.C., Larsen, P.E., Kennedy, K.S., Chien, H.-H., Lee, J.W. & Wen, H.B. (2013) Bone ingrowth and initial stability of titanium and porous tantalum dental implants: a pilot canine study. Implant dentistry 22: 399–405.
- Kim, J.H., Park, Y.B., Li, Z., Shim, J.S., Moon, H.S., Jung, H.S. & Chung, M.K. (2011) Effect of alendronate on healing of extraction sockets and healing around implants. Oral Diseases 17: 705–711.
- Lelovas, P.P., Xanthos, T.T., Thoma, S.E., Lyritis, G.P. & Dontas, I.A. (2008) The laboratory rat as an animal model for osteoporosis research. Comparative Medicine 58: 424–430.
- Li, L.-H., Kong, Y.-M., Kim, H.-W., Kim, Y.-W., Kim, H.-E., Heo, S.-J. & Koak, J.-Y. (2004) Improved biological performance of Ti implants due to surface modification by micro-arc oxidation. Biomaterials 25: 2867–2875.
- Lin, Z., Rios, H.F., Volk, S.L., Sugai, J.V., Jin, Q. & Giannobile, W.V. (2011) Gene expression dynamics during bone healing and osseointegration. Journal of periodontology 82: 1007–1017.
- Liu, X.L., Li, C.L., Lu, W.W., Cai, W.X. & Zheng, L.W. (2014) Skeletal site-specific response to ovariectomy in a rat model: change in bone density and microarchitecture. Clinical Oral Implants Research 26: 392–398.
- Luippold, G., Klein, T., Mark, M. & Grempler, R. (2012) Empagliflozin, a novel potent and selective SGLT-2 inhibitor, improves glycaemic control alone and in combination with insulin in streptozotocin-induced diabetic rats, a model of type 1 diabetes mellitus. Diabetes, Obesity and Metabolism 14: 601–607.
- Maimoun, L., Couret, I., Micallef, J.P., Peruchon, E., Mariano-Goulart, D., Rossi, M., Leroux, J.L. & Ohanna, F. (2002) Use of bone biochemical markers with dual-energy X-ray absorptiometry for early determination of bone loss in persons with spinal cord injury. Metabolism 51: 958–963.
- Morris, H.F., Ochi, S. & Winkler, S. (2000) Implant survival in patients with type 2 diabetes: placement to 36 months. Annals of Periodontology 5: 157–165.
- Mosekilde, L., Kragstrup, J. & Richards, A. (1987) Compressive strength, ash weight, and volume of vertebral trabecular bone in experimental fluorosis in pigs. Calcified Tissue International 40: 318–322.
- Mosekilde, L., Weisbrode, S.E., Safron, J.A., Stills, H.F., Jankowsky, M.L., Ebert, D.C., Danielsen, C.C., Sogaard, C.H., Franks, A.F., Stevens, M.L., Paddock, C.L. & Boyce, R.W. (1993) Calcium-restricted ovariectomized Sinclair S-1 minipigs: an animal model of osteopenia and trabecular plate perforation. Bone 14: 379–382.
- Nagasawa, M., Takano, R., Maeda, T. & Uoshima, K. (2013) Observation of the bone surrounding an overloaded implant in a novel rat model. The International Journal of Oral & Maxillofacial Implants 28: 109–116.
- Oliveira, P.A.D., Oliveira, A.M.S.D., Pablos, A.B., Costa, F.O., Silva, G.A.B., Santos, J.N.D. & Cury, P.R. (2012) Influence of hyperbaric oxygen therapy on peri-implant bone healing in rats with alloxan-induced diabetes. Journal of Clinical Periodontology 39: 879–886.
- Olsen, B.R., Reginato, A.M. & Wang, W. (2000) Bone development. Annual Review of Cell and Developmental Biology 16: 191–220.
- Park, R., Kim, J.H., Choi, H., Park, Y.B., Jung, H.S. & Moon, H.S. (2013) Effect of alendronate on bone remodeling around implant in the rat. The Journal of Advanced Prosthodontics 5: 374–381.
- Pearce, A., Richards, R., Milz, S., Schneider, E. & Pearce, S. (2007) Animal models for implant biomaterial research in bone: a review. European Cells & Materials 13: 1–10.
- Piattelli, A., Corigliano, M., Scarano, A., Costigliola, G. & Paolantonio, M. (1998) Immediate loading of titanium plasma-sprayed implants: an histologic analysis in monkeys. Journal of Periodontology 69: 321–327.
- Rawlinson, S.C., McKay, I.J., Ghuman, M., Wellmann, C., Ryan, P., Prajaneh, S., Zaman, G., Hughes, F.J. & Kingsmill, V.J. (2009) Adult rat bones maintain distinct regionalized expression of markers associated with their development. PLoS ONE 4: e8358.
- Rupp, F., Scheideler, L., Olshanska, N., De Wild, M., Wieland, M. & Geis-Gerstorfer, J. (2006) Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. Journal of Biomedical Materials Research Part A 76: 323–334.
- Schlegel, K.A., Prechtl, C., Most, T., Seidl, C., Lutz, R. & von Wilmowsky, C. (2013) Osseointegration of slactive implants in diabetic pigs. Clinical Oral Implants Research 24: 128–134.
- Sengupta, P. (2013) The laboratory rat: relating its age with human's. International Journal of Preventive Medicine 4: 624–630.
- Shirakura, M., Fujii, N., Ohnishi, H., Taguchi, Y., Ohshima, H., Nomura, S. & Maeda, T. (2003) Tissue response to titanium implantation in the rat maxilla, with special reference to the effects of surface conditions on bone formation. Clinical Oral Implants Research 14: 687–696.
- Soboku, K., Kikuchi, T., Fujita, S., Takeda, H., Naruse, K., Matsubara, T. & Noguchi, T. (2014) Altered gene expression in gingival tissues and enhanced bone loss in rats with diabetes with experimental periodontitis. Journal of Periodontology 85: 455–464.
- Thorwarth, M., Schultze-Mosgau, S., Kessler, P., Wiltfang, J. & Schlegel, K.A. (2005) Bone regeneration in osseous defects using a resorbable nanoparticular hydroxyapatite. Journal of Oral and Maxillofacial Surgery 63: 1626–1633.
- Tsolaki, I.N., Madianos, P.N. & Vrotsos, J.A. (2009) Outcomes of dental implants in osteoporotic patients. A literature review. Journal of Prosthodontics 18: 309–323.
- Turner, A., Maillet, J., Mallinckrodt, C. & Cordain, L. (1997) Bone mineral density of the skull in premenopausal women. Calcified Tissue International 61: 110–113.
- Van den Bos, T., Speijer, D., Bank, R., Brömme, D. & Everts, V. (2008) Differences in matrix composition between calvaria and long bone in mice suggest differences in biomechanical properties and resorption: special emphasis on collagen. Bone 43: 459–468.
- Vatsa, A., Breuls, R.G., Semeins, C.M., Salmon, P.L., Smit, T.H. & Klein-Nulend, J. (2008) Osteocyte morphology in fibula and calvaria – is there a role for mechanosensing? Bone 43: 452–458.
- Vico, L., Bourrin, S., Very, J.M., Radziszowska, M., Collet, P. & Alexandre, C. (1995) Bone changes in 6-mo-old rats after head-down suspension and a reambulation period. Journal of Applied Physiology 79: 1426–1433.
- Viera-Negron, Y.E., Ruan, W.H., Winger, J.N., Hou, X., Sharawy, M.M. & Borke, J.L. (2008) Effect of ovariectomy and alendronate on implant osseointegration in rat maxillary bone. The Journal of Oral Implantology 34: 76–82.
- Vigano, P., Botticelli, D., Salata, L.A., Schweikert, M.T., Urbizo Velez, J. & Lang, N.P. (2014) Healing at implant sites prepared conventionally or by means of sonosurgery. An experimental study in dogs. Clinical Oral Implants Research 26: 377–382.
- Vlaminck, L., Gorski, T., Huys, L., Saunders, J., Schacht, E. & Gasthuys, F. (2008) Immediate postextraction implant placement in sheep's mandibles: a pilot study. Implant Dentistry 17: 439–450.
- Yu, N., Oortgiesen, D.A., Bronckers, A.L., Yang, F., Walboomers, X.F. & Jansen, J.A. (2013) Enhanced periodontal tissue regeneration by periodontal cell implantation. Journal of Clinical Periodontology 40: 698–706.