Selection of animal models simulating the human jawbone for in vivo experiments on oral implants

doi:10.12337/zgkqzzxzz.2023.08.013

Abstract

Abstract: With the improvement of our national living standard and the popularization of dental implant technology, dental implants have become the first choice for the restoration of partially or completely edentulous jaws. To improve the surgical skill level of clinicians and develop excellent implants are important measures to improve the success rate of implant restorations, and neither physician training nor new implant development can be accomplished without preclinical experiments on animal models. Therefore, this paper reviews the animals and animal models suitable for dental implant surgery. The results of literature analysis show that there are a variety of animals that can be used to simulate the human jawbone for implant surgery or for testing the new implants developed. Pigs are the closest animal model to the human jawbone in terms of feeding habits, ethical considerations, physical size, temperament, structural characteristics, tissue composition, and bone remodeling of the jawbone tissue. However, due to the different experimental purposes, different animal models can be selected to carry out experiments. Additionally, an array of animal models can be concurrently employed to meet diverse research needs and achieve clinical treatment objectives.

Key words: Implant surgery, Animal model, Implant

Wang Qi, Teng Weiwei, Su Tianyue, Shu Qianyi, Li Cuiying, Wang Xinyu, Zhou Libo. Selection of animal models simulating the human jawbone for in vivo experiments on oral implants[J]. Chinese Journal of Oral Implantology, 2023, 28(4): 285-289.

References

[1] Hebel K, Gajjar R, Hofstede T.Single-tooth replacement: bridge vs. implant-supported restoration[J]. J Can Dent Assoc, 2000,66(8):435-438.
[2] Liaw K, Delfini RH, Abrahams JJ.Dental implant complications[J]. Semin Ultrasound CT MR, 2015, 36(5): 427-433. DOI: 10.1053/j.sult.2015.09.007.
[3] Liu CF, Lee TH, Liu JF, et al.A unique hybrid-structured surface produced by rapid electrochemical anodization enhances bio-corrosion resistance and bone cell responses of β-type Ti-24Nb-4Zr-8Sn alloy[J]. Sci Rep, 2018,8(1):6623. DOI: 10.1038/s41598-018-24590-x.
[4] Shi L, Shi L, Wang L, et al.The improved biological performance of a novel low elastic modulus implant[J]. PLoS One, 2013,8(2):e55015. DOI: 10.1371/journal.pone.0055015.
[5] Nune KC, Misra RD, Li SJ, et al.Cellular response of osteoblasts to low modulus Ti-24Nb-4Zr-8Sn alloy mesh structure[J]. J Biomed Mater Res A, 2017,105(3):859-870. DOI: 10.1002/jbm.a.35963.
[6] Bai Y, Hao YL, Li SJ, et al.Corrosion behavior of biomedical Ti-24Nb-4Zr-8Sn alloy in different simulated body solutions[J]. Mater Sci Eng C Mater Biol Appl, 2013,33(4):2159-2167. DOI: 10.1016/j.msec.2013.01.036.
[7] 朱睿, 刘蔚晴, 张鹏, 等. 种植体周围炎小鼠模型的研究进展[J].四川大学学报(医学版), 2020,51(6):767-770. DOI: 10.12182/20201160205.
[8] Wang YN, Jia TT, Feng Y, et al.Hyperlipidemia impairs osseointegration via the ROS/Wnt/β-catenin pathway[J]. J Dent Res, 2021,100(6):658-665. DOI: 10.1177/0022034520983245.
[9] King S, Klineberg I, Levinger I, et al.The effect of hyperglycaemia on osseointegration: a review of animal models of diabetes mellitus and titanium implant placement[J]. Arch Osteoporos, 2016,11(1):29. DOI: 10.1007/s11657-016-0284-1.
[10] 郝思维, 丁柏辰, 刘梦蝶, 等. 牙周炎实验动物的口腔解剖生理结构与模型建立[J].中国实用口腔科杂志, 2023, 16(1):104-109. DOI: 10.19538/j.kq.2023.01.018.
[11] 李洁, 刘仰, 陈雪英, 等. 颌骨放射性骨坏死动物模型的研究进展[J].口腔医学, 2018,38(4):372-375. DOI: 10.13591/j.cnki.kqyx.2018.04.018.
[12] Schimandle JH, Boden SD.Spine update. The use of animal models to study spinal fusion[J]. Spine (Phila Pa 1976), 1994,19(17):1998-2006. DOI: 10.1097/00007632-199409000-00023.
[13] Pearce AI, Richards RG, Milz S, et al.Animal models for implant biomaterial research in bone: a review[J]. Eur Cell Mater, 2007,13:1-10. DOI: 10.22203/ecm.v013a01.
[14] McGovern JA, Griffin M, Hutmacher DW. Animal models for bone tissue engineering and modelling disease[J]. Dis Model Mech, 2018,11(4):dmm033084.DOI: 10.1242/dmm.033084.
[15] Reichert JC, Saifzadeh S, Wullschleger ME, et al.The challenge of establishing preclinical models for segmental bone defect research[J]. Biomaterials, 2009,30(12):2149-2163. DOI: 10.1016/j.biomaterials.2008.12.050.
[16] Hazzard DG, Bronson RT, McClearn GE, et al. Selection of an appropriate animal model to study aging processes with special emphasis on the use of rat strains[J]. J Gerontol, 1992,47(3):B63-B64. DOI: 10.1093/geronj/47.3.b63.
[17] Blanc-Sylvestre N, Bouchard P, Chaussain C, et al.Pre-clinical models in implant dentistry: past, present, future[J]. Biomedicines, 2021,9(11):1538.DOI: 10.3390/biomedicines9111538.
[18] Schroeder HE, Lindhe J.Conversion of stable established gingivitis in the dog into destructive periodontitis[J]. Arch Oral Biol, 1975,20(12):775-782. DOI: 10.1016/0003-9969(75)90052-7.
[19] Ericsson I, Lindhe J, Rylander H, et al.Experimental periodontal breakdown in the dog[J]. Scand J Dent Res, 1975,83(3):189-192. DOI: 10.1111/j.1600-0722.1975.tb01198.x.
[20] Syed SA, Svanberg M, Svanberg G.The predominant cultivable dental plaque flora of beagle dogs with periodontitis[J]. J Clin Periodontol, 1981,8(1):45-56. DOI: 10.1111/j.1600-051x.1981.tb02023.x.
[21] Pellegrini G, Seol YJ, Gruber R, et al.Pre-clinical models for oral and periodontal reconstructive therapies[J]. J Dent Res, 2009,88(12):1065-1076. DOI: 10.1177/0022034509349748.
[22] Berglundh T, Lindhe J, Marinello C, et al.Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog[J]. Clin Oral Implants Res, 1992,3(1):1-8.
[23] Zitzmann NU, Berglundh T, Ericsson I, et al.Spontaneous progression of experimentally induced periimplantitis[J]. J Clin Periodontol, 2004,31(10):845-849. DOI: 10.1111/j.1600-051X.2004.00567.x.
[24] Kimmel DB, Jee WS.A quantitative histologic study of bone turnover in young adult beagles[J]. Anat Rec, 1982,203(1):31-45. DOI: 10.1002/ar.1092030104.
[25] Wang X, Mabrey JD, Agrawal CM.An interspecies comparison of bone fracture properties[J]. Biomed Mater Eng, 1998,8(1):1-9.
[26] Koschmieder R, Ritzerfield W, Homeyer L.Addition of gentamicine to polymethyl methacrylate for therapy of infectious bone diseases. expeimental in vivo tests[J]. Z Orthop Ihre Grenzgeb, 1975,113(1):147-149.
[27] Swindle MM, Makin A, Herron AJ, et al.Swine as models in biomedical research and toxicology testing[J]. Vet Pathol, 2012,49(2):344-356. DOI: 10.1177/0300985811402846.
[28] Buser D, Schenk RK, Steinemann S, et al.Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs[J]. J Biomed Mater Res, 1991,25(7):889-902. DOI: 10.1002/jbm.820250708.
[29] Wang S, Liu Y, Fang D, et al.The miniature pig: a useful large animal model for dental and orofacial research[J]. Oral Dis, 2007,13(6):530-537. DOI: 10.1111/j.1601-0825.2006.01337.x.
[30] von Wilmowsky C, Stockmann P, Metzler P, et al. Establishment of a streptozotocin-induced diabetic domestic pig model and a systematic evaluation of pathological changes in the hard and soft tissue over a 12-month period[J]. Clin Oral Implants Res, 2010,21(7):709-717. DOI: 10.1111/j.1600-0501.2010.01914.x.
[31] Raab DM, Crenshaw TD, Kimmel DB, et al.A histomorphometric study of cortical bone activity during increased weight-bearing exercise[J]. J Bone Miner Res, 1991,6(7):741-749. DOI: 10.1002/jbmr.5650060712.
[32] Aerssens J, Boonen S, Lowet G, et al.Interspecies differences in bone composition, density, and quality: potential implications for in vivo bone research[J]. Endocrinology, 1998,139(2):663-670. DOI: 10.1210/endo.139.2.5751.
[33] Mosekilde L, Kragstrup J, Richards A.Compressive strength, ash weight, and volume of vertebral trabecular bone in experimental fluorosis in pigs[J]. Calcif Tissue Int, 1987,40(6):318-322. DOI: 10.1007/BF02556693.
[34] Reichert JC, Saifzadeh S, Wullschleger ME, et al.The challenge of establishing preclinical models for segmental bone defect research[J]. Biomaterials, 2009,30(12):2149-2163. DOI: 10.1016/j.biomaterials.2008.12.050.
[35] Wancket LM.Animal models for evaluation of bone implants and devices: comparative bone structure and common model uses[J]. Vet Pathol, 2015,52(5):842-850. DOI: 10.1177/0300985815593124.
[36] Leung KS, Siu WS, Cheung NM, et al.Goats as an osteopenic animal model[J]. J Bone Miner Res, 2001,16(12):2348-2355. DOI: 10.1359/jbmr. 2001. 16.12.2348.
[37] Anderson ML, Dhert WJ, de Bruijn JD, et al. Critical size defect in the goat's os ilium. A model to evaluate bone grafts and substitutes[J]. Clin Orthop Relat Res, 1999,(364):231-239. DOI: 10.1097/00003086-199907000-00030.
[38] van der Donk S, Buma P, Aspenberg P, et al. Similarity of bone ingrowth in rats and goats: a bone chamber study[J]. Comp Med, 2001,51(4):336-340.
[39] Ravaglioli A, Krajewski A, Celotti GC, et al.Mineral evolution of bone[J]. Biomaterials, 1996,17(6):617-622. DOI: 10.1016/0142-9612(96)88712-6.
[40] Spaargaren DH.Metabolic rate and body size: a new view on the 'surface law' for basic metabolic rate[J]. Acta Biotheor, 1994,42(4):263-269. DOI: 10.1007/BF00707392.
[41] Liebschner MA.Biomechanical considerations of animal models used in tissue engineering of bone[J]. Biomaterials, 2004,25(9):1697-1714. DOI: 10.1016/s0142-9612(03)00515-5.
[42] Neyt JG, Buckwalter JA, Carroll NC.Use of animal models in musculoskeletal research[J]. Iowa Orthop J, 1998,18:118-123.
[43] Mori H, Manabe M, Kurachi Y, et al. Osseointegration of dental implants in rabbit bone with low mineral density[J]. J Oral Maxillofac Surg, 1997,55(4):351-361, discussion 362. DOI: 10.1016/s0278-2391(97)90124-5.
[44] Vignoletti F, Abrahamsson I.Quality of reporting of experimental research in implant dentistry. critical aspects in design, outcome assessment and model validation[J]. J Clin Periodontol, 2012,39(Suppl 12):S6-S27. DOI: 10.1111/j.1600-051X.2011.01830.x.
[45] Gilsanz V, Roe TF, Gibbens DT, et al.Effect of sex steroids on peak bone density of growing rabbits[J]. Am J Physiol, 1988,255(4 Pt 1):e416-e421. DOI: 10.1152/ajpendo.1988.255.4.E416.
[46] Brewer NR.Biology of the rabbit[J]. J Am Assoc Lab Anim Sci, 2006,45(1):8-24.
[47] Martiniaková M, Grosskopf B, Omelka R, et al.Differences among species in compact bone tissue microstructure of mammalian skeleton: use of a discriminant function analysis for species identification[J]. J Forensic Sci, 2006,51(6):1235-1239. DOI: 10.1111/j.1556-4029.2006.00260.x.