Tissue Engineering and Regenerative Medicine

Korean Tissue Engineering and Regenerative Medicine Society (한국조직공학·재생의학회)
권호 표지
DOI QR코드

DOI QR Code

Rat Defect Models for Bone Grafts and Tissue Engineered Bone Constructs

  • Kim, Joong-Hyun (Institute of Tissue Regeneration Engineering (ITREN), Dankook University) ;
  • Kim, Hae-Won (Institute of Tissue Regeneration Engineering (ITREN), Dankook University)
  • Received : 2013.05.06
  • Accepted : 2013.07.01
  • Published : 2013.12.01
⟨ Previous Next ⟩

Abstract

The development of optimized biomaterials for restoring bone defects has been ongoing for many years. Animal models for testing bone grafts and tissue engineered constructs are an important aspect of this research. New bone scaffolding systems need to be tested both in vitro and in vivo, but ultimately animal studies provide answers and confidence in their efficacy prior to clinical applications. A robust set of rat models for understanding bone development in response to implanted materials have been developed. This review will describe frequently used rat bone defect models, such as the calvarial defect, long bone defect, and maxillofacial bone defect models.

Keywords

References

  1. JR Porter, TT Ruckh, KC Popat, Bone tissue engineering: a review in bone biomimetics and drug delivery strategies, Biotechnol Prog, 25, 1539 (2009).
  2. SV Dorozhkin, Calcium orthophosphates as bioceramics-state of the art, J Funct Biomater, 1, 22 (2010). https://doi.org/10.3390/jfb1010022
  3. WT Godbey, A Atala, In vitro systems for tissue engineering, Ann N Y Acad Sci, 961, 1 (2002). https://doi.org/10.1111/j.1749-6632.2002.tb03040.x
  4. AI Pearce, RG Richards, S Milz, et al., Animal models for implant biomaterial research in bone, Eur Cell Mater, 2, 1 (2007).
  5. M Viceconti, R Muccini, M Bernakiewicz, et al., Largesliding contact elements accurately predict levels of boneimplant micromotion relevant to osseointegration, J Biomech, 33, 1611 (2000). https://doi.org/10.1016/S0021-9290(00)00140-8
  6. M Geetha, AK Singh, R Asokamani, et al., Ti based biomaterials, the ultimate choice for orthopaedic implants-a review, Prog in Mater Sci, 54, 397 (2009). https://doi.org/10.1016/j.pmatsci.2008.06.004
  7. MB Nasab, MR Hassan, Metallic biomaterials of knee and hip-a review, Trends Biomater Artif Organs, 24, 69 (2010).
  8. F Peters, D Reif, Functional materials for bone regeneration from beta tricalcium phosphate, Materwiss Werksttech, 35, 203 (2004). https://doi.org/10.1002/mawe.200400735
  9. B Schroder, S Vossing, G Breves, In vitro studies on active calcium absorption from ovine rumen, J Comp Physiol B, 169, 487 (1999). https://doi.org/10.1007/s003600050246
  10. S Reinwald, D Burr, Review of nonprimate, large animal models for osteoporosis research, J Bone Miner Res, 23, 1353 (2008). https://doi.org/10.1359/jbmr.080516
  11. G Pellegrini, YJ Seol, R Gruber, et al., Pre-clinical models for oral and periodontal reconstructive therapies, J Dent Res, 88, 1065 (2009). https://doi.org/10.1177/0022034509349748
  12. DR Sumner, TM Turner, RM Urban, Animal models relevant to cementless joint replacement, J Musculoskelet Neuronal Interact, 1, 333 (2001).
  13. P O'Loughlin, S Morr, L Bogunovic, et al., Selection and development of preclinical models in fracture-healing research, J Bone Joint Surg Am, 90, 79 (2008). https://doi.org/10.2106/JBJS.G.01585
  14. M Egermann, J Goldhahn, E Schneider, Animal models for fracture treatment in osteoporosis, Osteoporos Int, 16, S129 (2005). https://doi.org/10.1007/s00198-005-1859-7
  15. SR Sheng, XY Wang, HZ Xu, et al., Anatomy of large animal spines and its comparison to the human spine: a systematic review, Eur Spine J, 19, 46 (2010). https://doi.org/10.1007/s00586-009-1192-5
  16. PS Gomes, MH Fernandes, Rodent models in bone-related research: the relevance of calvarial defects in the assessment of bone regeneration strategies, Lab Anim, 45, 14 (2011). https://doi.org/10.1258/la.2010.010085
  17. MA Liebschner, Biomechanical considerations of animal models used in tissue engineering of bone, Biomaterials, 25, 1697 (2004). https://doi.org/10.1016/S0142-9612(03)00515-5
  18. V Cacciafesta, M Dalstra, C Bosch, et al., Growth hormone treatment promotes guided bone regeneration in rat calvarial defects, Eur J Orthod, 23, 733 (2001). https://doi.org/10.1093/ejo/23.6.733
  19. C Szpalski, J Barr, M Wetterau, et al., Cranial bone defects: current and future strategies, Neurosurg Focus, 29, E8 (2010).
  20. A Cacchioli, B Spaggiari, F Ravanetti, et al., The critical sized bone defect: morphological study of bone healing, Ann Fac Medic Vet di Parma, XXVI, 97 (2006).
  21. D Ozcelik, T Turan, F Kabukcuoolu, et al., Bone induction capacity of the periosteum and neonatal dura in the setting of the rat zygomatic arch fracture model, Arch Facial Plast Surg, 5, 301 (2003). https://doi.org/10.1001/archfaci.5.4.301
  22. J Mah, J Hung, J Wang, et al., The efficacy of various alloplastic bone grafts on the healing of rat calvarial defects, Eur J Orthod, 26, 475 (2004). https://doi.org/10.1093/ejo/26.5.475
  23. E Yoon, S Dhar, DE Chun, et al., In vivo osteogenic potential of human adipose-derived stem cells/poly lactide-co-glycolic acid constructs for bone regeneration in a rat critical-sized calvarial defect model, Tissue Eng, 13, 619 (2007). https://doi.org/10.1089/ten.2006.0102
  24. T Itagaki, T Honma, I Takahashi, et al., Quantitative analysis and localization of mRNA transcripts of type I collagen, osteocalcin, MMP 2, MMP 8, and MMP 13 during bone healing in a rat calvarial experimental defect model, Anat Rec (Hoboken), 291, 1038 (2008). https://doi.org/10.1002/ar.20717
  25. H Develioglu, S Unver Saraydin, U Kartal, The bone-healing effect of a xenograft in a rat calvarial defect model, Dent Mater J, 28, 396 (2009). https://doi.org/10.4012/dmj.28.396
  26. GF Muschler, VP Raut, TE Patterson, et al., The design and use of animal models for translational research in bone tissue engineering and regenerative medicine, Tissue Eng Part B Rev, 16, 123 (2010).
  27. E Freeman, RS Turnbull, The value of osseous coagulum as a graft material, J Periodontal Res, 8, 229 (1973). https://doi.org/10.1111/j.1600-0765.1973.tb00762.x
  28. JB Mulliken, J Glowacki, Induced osteogenesis for repair and construction in the craniofacial region, Plast Reconstr Surg, 65, 553 (1980). https://doi.org/10.1097/00006534-198005000-00001
  29. C Dahlin, P Alberius, A Linde, Osteopromotion for cranioplasty. An experimental study in rats using a membrane technique, J Neurosurg, 74, 487 (1991). https://doi.org/10.3171/jns.1991.74.3.0487
  30. A Linde, C Thorén, C Dahlin, et al., Creation of new bone by an osteopromotive membrane technique: an experimental study in rats, J Oral Maxillofac Surg, 51, 892 (1993). https://doi.org/10.1016/S0278-2391(10)80111-9
  31. C Bosch, B Melsen, K Vargervik, Importance of the critical-size bone defect in testing bone-regenerating materials, J Craniofac Surg, 9, 310 (1998). https://doi.org/10.1097/00001665-199807000-00004
  32. K Takagi, MR Urist, The reaction of the dura to bone morphogenetic protein (BMP) in repair of skull defects, Ann Surg, 196, 100 (1982). https://doi.org/10.1097/00000658-198207000-00020
  33. JP Schmitz, Z Schwartz, JO Hollinger, et al., Characterization of rat calvarial nonunion defects, Acta Anat (Basel), 138, 185 (1990). https://doi.org/10.1159/000146937
  34. JP Schmitz, JO Hollinger, The critical size defect as an experimental model for craniomandibulofacial nonunions, Clin Orthop Relat Res, 205, 299 (1986).
  35. SM Bidic, JW Calvert, K Marra, Rabbit calvarial wound healing by means of seeded $Caprotite^{(R)}$ scaffolds, J Dent Res, 82, 131 (2003). https://doi.org/10.1177/154405910308200211
  36. CF Mossaz, VG Kokich, Redevelopment of the calvaria after partial craniectomy in growing rabbits: the effect of altering dural continuity, Acta Anat (Basel), 109, 321 (1981). https://doi.org/10.1159/000145398
  37. MR Urist, BF Silverman, K Büring, et al., The bone induction principle, Clin Orthop, 53, 243 (1967).
  38. L Uddströmer, V Ritsilä, Healing of membranous and long bone defects. An experimental study in growing rabbits, Scand J Plast Reconstr Surg, 13, 281 (1979). https://doi.org/10.3109/02844317909013071
  39. JC Yu, JS McClintock, F Gannon, et al., Regional differences of dura osteoinduction: squamous dura induces osteogenesis, sutural dura induces chondrogenesis and osteogenesis, Plast Reconstr Surg, 100, 23 (1997). https://doi.org/10.1097/00006534-199707000-00005
  40. B Mehrara, D Most, J Chang, et al., Basic fibroblast growth factor and transforming growth factor â-1 expression in the developing dura mater correlates with calvarial bone formation, Plast Reconstr Surg, 104, 435 (1999). https://doi.org/10.1097/00006534-199908000-00017
  41. P Buma, W Schreurs, N Verdonschot, Skeletal tissue engineering-from in vitro studies to large animal models, Biomaterials, 25, 1487 (2004). https://doi.org/10.1016/S0142-9612(03)00492-7
  42. L Le Guehennec, E Goyenvalle, E Aguado, et al., Small-animal models for testing macroporous ceramic bone substitutes, J Biomed Mater Res B Appl Biomater, 72, 69 (2005).
  43. S Karaoglu, A Baktir, S Kabak, et al., Experimental repair of segmental bone defects in rabbits by demineralized allograft covered by free autogenous periosteum, Injury, 33, 679 (2002). https://doi.org/10.1016/S0020-1383(02)00086-4
  44. S Kokubo, R Fujimoto, S Yoakta, et al., Bone regeneration by recombinant human bone morphogenetic protein-2 and a novel biodegradable carrier in a rabbit ulnar defect model, Biomaterials, 24, 1643 (2003). https://doi.org/10.1016/S0142-9612(02)00551-3
  45. HY Kim, BY Sohn, UK Seo, et al., An exploratory study of gold wire implantation at acupoints to accelerate ulnar fracture healing in rats, J Physiol Sci, 59, 329 (2009). https://doi.org/10.1007/s12576-009-0038-6
  46. E Solheim, EM Pinholt, R Andersen, et al., The effect of a composite of polyorthoester and demineralized bone on the healing of large segmental defects of the radius in rats, J Bone Joint Surg Am, 74, 1456 (1992). https://doi.org/10.2106/00004623-199274100-00004
  47. G Alper, S Bernick, M Yazdi, et al., Osteogenesis in bone defects in rats: the effects of hydroxyapatite and demineralized bone matrix, Am J Med Sci, 298, 371 (1989). https://doi.org/10.1097/00000441-198912000-00003
  48. A Roshan-Ghias, FM Lambers, M Gholam-Rezaee, et al., In vivo loading increases mechanical properties of scaffold by affecting bone formation and bone resorption rates, Bone, 49, 1357 (2011). https://doi.org/10.1016/j.bone.2011.09.040
  49. H Tsuchida, J Hashimoto, E Crawford, et al., Engineered allogeneic mesenchymal stem cells repair femoral segmental defect in rats, J Orthop Res, 21, 44 (2003). https://doi.org/10.1016/S0736-0266(02)00108-0
  50. MV Martins, MA da Silva, E Medici Filho, et al., Evaluation of digital optical density of bone repair in rats medicated with ketoprofen, Braz Dent J, 16, 207 (2005). https://doi.org/10.1590/S0103-64402005000300007
  51. AL Anbinder, JC Junqueira, MN Mancini, et al., Influence of simvastatin on bone regeneration of tibial defects and blood cholesterol level in rats, Braz Dent J, 17, 267 (2006). https://doi.org/10.1590/S0103-64402006000400001
  52. L Offer, B Veigel, T Pavlidis, et al., Phosphoserine-modified calcium phosphate cements: bioresorption and substitution, J Tissue Eng Regen Med, 5, 11 (2011). https://doi.org/10.1002/term.283
  53. SE Utvåg, KB Iversen, O Grundnes, et al., Poor muscle coverage delays fracture healing in rats, Acta Orthop Scand, 73, 471 (2002). https://doi.org/10.1080/00016470216315
  54. NJ Willett, MT Li, BA Uhrig, et al., Attenuated human bone morphogenetic protein-2-mediated bone regeneration in a rat model of composite bone and muscle injury, Tissue Eng Part C Methods, 19, 316 (2013).
  55. A Hulth, Current concepts of fracture healing, Clin Orthop Relat Res, 249, 265 (1989).
  56. DM Nunamaker, Experimental models of fracture repair, Clin Orthop Relat Res, 355 Suppl, S56 (1998).
  57. L Carlsson, T Rostlund, B Albrektsson, et al., Implant fixation improved by close fit. Cylindrical implant-bone interface studied in rabbits, Acta Orthop Scand, 59, 272 (1988). https://doi.org/10.3109/17453678809149361
  58. DA Garcia, TM Sullivan, DM O'Neill, The biocompatibility of dental implant materials measured in an animal model, J Dent Res, 60, 44 (1981). https://doi.org/10.1177/00220345810600010801
  59. JW Frame, A convenient animal model for testing bone substitute materials, J Oral Surg, 38, 176 (1980).
  60. OA Arosarena, WL Collins, Defect repair in the rat mandible with bone morphogenic protein 5 and prostaglandin E1, Arch Otolaryngol Head Neck Surg, 129, 1125 (2003). https://doi.org/10.1001/archotol.129.10.1125
  61. LJ Rever, PN Manson, MA Randolph, et al., The healing of facial bone fractures by the process of secondary union, Plast Reconstr Surg, 87, 451 (1991). https://doi.org/10.1097/00006534-199103000-00009
  62. SR Thaller, J Hoyt, H Tesluk, et al., Effect of insulin-like growth factor-1 on zygomatic arch bone regeneration: a preliminary histological and histometric study, Ann Plast Surg, 31, 421 (1993). https://doi.org/10.1097/00000637-199311000-00006
  63. MG Kim, DM Shin, SW Lee, The healing of critical-sized bone defect of rat zygomatic arch with particulate bone graft and bone morphogenetic protein-2, J Plast Reconstr Aesthet Surg, 63, 459 (2010). https://doi.org/10.1016/j.bjps.2008.11.081
  64. PD Nguyen, CD Lin, AC Allori, et al., Establishment of a critical-sized alveolar defect in the rat: a model for human gingivoperiosteoplasty, Plast Reconstr Surg, 123, 817 (2009). https://doi.org/10.1097/PRS.0b013e31819ba2f4
  65. BJ Mehrara, PB Saadeh, DS Steinbrech, et al., A rat model of gingivoperiosteoplasty, J Craniofac Surg, 11, 54 (2000). https://doi.org/10.1097/00001665-200011010-00010
  66. AH Melcher, Repair of wounds in the periodontium of the rat. Influence of periodontal ligament on osteogenesis, Arch Oral Biol, 15, 1183 (1970). https://doi.org/10.1016/0003-9969(70)90010-5
  67. B Klausen, Microbiological and immunological aspects of experimental periodontal disease in rats: a review article, J Periodontol, 62, 59 (1991). https://doi.org/10.1902/jop.1991.62.1.59
  68. JH Kim, MK Kim, JH Park, et al., Performance of novel nanofibrous biopolymer membrane for guided bone regeneration within rat mandibular defect, In Vivo, 25, 589 (2011).
  69. L Kostopoulos, T Karring, Augmentation of the rat mandible using guided tissue regeneration, Clin Oral Implants Res, 5, 75 (1994). https://doi.org/10.1034/j.1600-0501.1994.050203.x
  70. A Linde, E Hedner, Recombinant bone morphogenetic protein- 2 enhances bone healing, guided by osteopromotive e-PTFE membranes: an experimental study in rats, Calcif Tissue Int, 56, 549 (1995). https://doi.org/10.1007/BF00298588
  71. MB Guglielmotti, RL Cabrini, Alveolar wound healing and ridge remodeling after tooth extraction in the rat: a histologic, radiographic, and histometric study, J Oral Maxillofac Surg, 43, 359 (1985). https://doi.org/10.1016/0278-2391(85)90257-5
  72. MC Pereira, KG Zecchin, EB Campagnoli, et al., Ovariectomy delays alveolar wound healing after molar extractions in rats, J Oral Maxillofac Surg, 65, 2248 (2007). https://doi.org/10.1016/j.joms.2006.11.040

Cited by

  1. Effect of surface-treatments on flexibility and guided bone regeneration of titanium barrier membrane vol.25, pp.3, 2015, https://doi.org/10.6111/jkcgct.2015.25.3.098
  2. Blood Prefabrication Subcutaneous Small Animal Model for the Evaluation of Bone Substitute Materials vol.4, pp.7, 2018, https://doi.org/10.1021/acsbiomaterials.8b00323
  3. Animal models for bone tissue engineering and modelling disease vol.11, pp.4, 2013, https://doi.org/10.1242/dmm.033084
  4. Do electrical current and laser therapies improve bone remodeling during an orthodontic treatment with corticotomy? vol.23, pp.11, 2013, https://doi.org/10.1007/s00784-019-02845-9
  5. Rat sinus mucosa‐ and periosteum‐derived exosomes accelerate osteogenesis vol.234, pp.12, 2019, https://doi.org/10.1002/jcp.28758
  6. Octacalcium phosphate/gelatin composite facilitates bone regeneration of critical-sized mandibular defects in rats: A quantitative study vol.13, pp.4, 2013, https://doi.org/10.15171/joddd.2019.040
  7. The Efficacy of Recombinant Platelet-Derived Growth Factor on Beta-Tricalcium Phosphate to Regenerate Femoral Critical Sized Segmental Defects: Longitudinal In Vivo Micro-CT Study in a Rat Model vol.33, pp.5, 2020, https://doi.org/10.1080/08941939.2018.1519048
  8. Hydrogel as a Biomaterial for Bone Tissue Engineering: A Review vol.10, pp.8, 2013, https://doi.org/10.3390/nano10081511
  9. Effect of Stromal Vascular Fraction on Fracture Healing with Bone Defects by Examination of Bone Morphogenetic Protein-2 Biomarkers in Murine Model vol.9, pp.1, 2021, https://doi.org/10.3889/oamjms.2021.7385
  10. Reconstruction of critical‐size segmental defects in rat femurs using carbonate apatite honeycomb scaffolds vol.109, pp.9, 2013, https://doi.org/10.1002/jbm.a.37157
  11. Osteocalcin biomarker level evaluation on fracture healing with bone defect after stromal vascular fraction application in murine model vol.71, pp.None, 2021, https://doi.org/10.1016/j.amsu.2021.103020
  12. Decompression effects on bone healing in rat mandible osteomyelitis vol.11, pp.1, 2013, https://doi.org/10.1038/s41598-021-91104-7