A Reappraisal of Various Animal Models used in Periodontology with Future Perspectives and Alternatives

Download Article

DOI: 10.21522/TIJPH.2013.10.04.Art021

Authors : Sameena Parveen, Vinay Kumar

Abstract:

Periodontitis is an inflammatory infectious disease that occurs when the supporting tissues of the teeth are infected by a mix of gram-positive bacteria (GPB), and anaerobic bacteria. Periodontitis must be treated as soon as possible to avoid more injury and worsening of the condition. Prior to evaluating new treatments, animal studies are used in conjunction with in vitro studies in periodontitis research. Even though cultured cells can be used to examine physiological processes that occur in periodontitis development, the complex host response that is at the root of the illness is impossible to replicate in vitro. Mice, rats, rabbits, hamsters, nonhuman primates, dogs, and pigs have all been used to imitate human periodontitis, each with its own set of benefits and drawbacks. Animals have played an important part in researching periodontal diseases and developing effective treatments. There is a limitation in the usage of large animals due to their housing problems. Animals for periodontitis are selected based on their resemblance with that human structure and functioning. The usage of these animals will aid in the better and more precise replication of human disease. This will improve the disease’s prognosis and treatment outcome. As a result, the medications utilized can provide a better indication of the effect they will have on the human body based on the effects they have on animal models. Therefore, it is critical to use appropriate animals in periodontal research in order to develop improved treatments for these disorders. Thus, animal models play a crucial role in periodontal research.

Keywords: Animal models; Bacteria; In vitro; Periodontitis; Treatment.

References:

[1] Oz, H.S., Puleo, D.A., 2011, Animal models for periodontal disease. J Biomed Biotechnol., 2011:754857.

[2] Nazir, M., Al-Ansari, A., Al-Khalifa, K., Alhareky, M., Gaffar, B., Almas, K., 2020, Global Prevalence of Periodontal Disease and Lack of Its Surveillance. Scientific World Journal, 2146160.

[3] Relvas, M., López-Jarana, P., Monteiro, L., Pacheco, J.J., Braga, A.C., Salazar, F., 2022, Study of Prevalence, Severity and Risk Factors of Periodontal Disease in a Portuguese Population. J Clin Med., 11(13),3728.

[4] Reynolds, I., Duane, B., 2018, Periodontal disease has an impact on patients’ quality of life. Evidence-based dentistry, 19(1),14-5.

[5] Tonetti, M.S., Bottenberg, P., Conrads, G., Eickholz, P., Heasman, P., Huysmans, M.C., López, R., Madianos, P., Müller, F., Needleman, I., Nyvad B., 2017, Dental caries and periodontal diseases in the ageing population: call to action to protect and enhance oral health and well‐being as an essential component of healthy ageing–Consensus report of group 4 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. Journal of clinical periodontology, 44, S135-44.

[6] Pasupuleti, M.K., Molahally, S.S., Salwaji S., 2016, Ethical guidelines, animal profile, various animal models used in periodontal research with alternatives and future perspectives. Journal of Indian Society of Periodontology, 20(4),360.

[7] How, K.Y., Song, K.P., Chan K.G., 2016, Porphyromonasgingivalis: an overview of periodontopathic pathogen below the gum line. Frontiers in microbiology, 9(7), 53.

[8] Cekici, A., Kantarci, A., Hasturk, H., Van Dyke, T.E., 2014, Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontology 2000, 64(1), 57-80.

[9] Zhou, L.N., Bi, C.S., Gao, L.N., An, Y., Chen, F., Chen, F.M., 2019, Macrophage polarization in human gingival tissue in response to periodontal disease. Oral diseases, 25(1), 265-73.

[10] Ausenda, F., Rasperini, G., Acunzo, R., Gorbunkova, A., Pagni, G.,2019, New perspectives in the use of biomaterials for periodontal regeneration. Materials, 12(13), 2197.

[11] Xu, X.Y., Li, X., Wang, J., He, X.T., Sun, H.H., Chen, F.M.,2019, Concise review: periodontal tissue regeneration using stem cells: strategies and translational considerations. Stem cells translational medicine, 8(4), 392-403.

[12] Struillou, X., Boutigny, H., Soueidan, A., Layrolle, P.,2010, Experimental animal models in periodontology: a review. The open dentistry journal, 4, 37.

[13] Martínez-García, M., Hernández-Lemus, E., 2021, Periodontal inflammation and systemic diseases: an overview. Frontiers in physiology, 1842.

[14] Gonzalez, OA., Nagarajan, R., Novak, M.J, Orraca, L., Gonzalez‐Martinez, JA., Kirakodu, S.S., Ebersole, J.L., 2016, Immune system transcriptome in gingival tissues of young nonhuman primates. Journal of periodontal research, 51(2), 152-63.

[15] Dannan, A., Alkattan, F., 2007, Animal models in periodontal research: A mini review of the literature. The Internet Journal of Veterinary Medicine, 5(1), 5.

[16] Liang, Y., Luan, X., Liu, X., 2020, Recent advances in periodontal regeneration: A biomaterial perspective, Bioactive materials, 5(2), 297-308.

[17] Sulijaya, B., Rahdewati, H., Sunarto, H., Soeroso, Y., 2019, An. Maximizing Periodontal Defect Creation and Experimental Design in Non-Human Primate Model Study. An Updated Review Article Journal of International Dental and Medical Research, 12(2), 733-7.

[18] Kantarci, A., Hasturk, H., Van, Dyke., T.E., 2015, Animal models for periodontal regeneration and peri‐implant responses. Periodontology 2000, 68(1), 66-82.

[19] Shanbhag, S., Pandis, N., Mustafa, K., Nyengaard, J.R., Stavropoulos, A., 2017, Alveolar bone tissue engineering in critical‐size defects of experimental animal models: a systematic review and meta‐analysis. Journal of tissue engineering and regenerative medicine,11(10), 2935-49.

[20] Li, D., Feng, Y., Tang, H., Huang, L., Tong, Z., Hu, C., Chen, X., Tan, J.,2020, A simplified and effective method for generation of experimental murine periodontitis model. Frontiers in Bioengineering and Biotechnology, 25(8),444.

[21] Marchesan, J., Girnary, MS., Jing, L., Miao, M.Z., Zhang, S., Sun, L., Morelli, T., Schoenfisch, M.H., Inohara, N., Offenbacher, S., Jiao, Y.,2018, An experimental murine model to study periodontitis. Nature protocols,13(10), 2247-67.

[22] Bhattarai, G., Poudel, SB., Kook, S.H, Lee, J.C.,2016, Resveratrol prevents alveolar bone loss in an experimental rat model of periodontitis. Acta biomaterialia,1(29),398-408.

[23] Courbon, G., Rinaudo-Gaujous, M., Blasco-Baque, V., Auger, I., Caire, R., Mijola, L., Vico, L., Paul, S., Marotte, H., 2019, Porphyromonasgingivalis experimentally induces periodontitis and an anti-CCP2-associated arthritis in the rat. Annals of the rheumatic diseases, 78(5), 594-9.

[24] Offenbacher, S., Jiao, Y., Kim, SJ., Marchesan, J., Moss, K.L., Jing, L., Divaris, K., Bencharit, S., Agler, C.S., Morelli, T., Zhang, S.,2018, GWAS for Interleukin-1β levels in gingival crevicular fluid identifies IL37 variants in periodontal inflammation. Nature communications, 9(1), 1-7.

[25] Fawzy, El-Sayed., K.M, Doerfer., C.E., 2017, Animal models for periodontal tissue engineering: a knowledge-generating process. Tissue Engineering Part C: Methods, 23(12), 900-25.

[26] Donos, N., Park, J.C., Vajgel, A., de, Carvalho, Farias, B., Dereka, X., 2018, Description of the periodontal pocket in preclinical models: limitations and considerations. Periodontology 2000, 76(1), 16-34.

[27] Jati, A.S., Furquim, L.Z., Consolaro, A., 2016, Gingival recession: its causes and types, and the importance of orthodontic treatment. Dental press journal of orthodontics, 21,18-29.

[28] Preshaw, P.M., 2015, Detection and diagnosis of periodontal conditions amenable to prevention. BMC oral health, 15(1),1-1.

[29] Dahlén, G., Charalampakis, G., Abrahamsson, I., Bengtsson, L., Falsen, E., 2012, Predominant bacterial species in subgingival plaque in dogs. Journal of periodontal research, 47(3), 354-64.

[30] Nicholls, V.M., Townsend, N., 2016, Dental disease in aged horses and its management. Veterinary Clinics: Equine Practice, 32(2), 215-27.

[31] Tyrrell, K.L., Citron, D.M., Jenkins, J.R., Goldstein, E.J., 2002, Periodontal bacteria in rabbit mandibular and maxillary abscesses. J Clin Microbiol., 40(3):1044-7.

[32] Banu, S.R., J., 2018, A Review Role of Animal Models in Periodontal Research. Asian Journal of Pharmaceutical and Clinical Research, 11(7),47-51.

[33] Schou, S., Holmstrup, P., Kornman, KS., 1993, A review of the literature non-human primates used in studies of periodontal disease pathogenesis. J Periodontol, 64,497-508.

[34] Priyanka, M., Jaiganesh, D.R.,2013, Periodontally accelerated osteogenic orthodontics. Int J Pharm PharSci, 5,49-51.

[35] Giannobile, W.V., Finkelman, R.D., Lynch, S.E., 1994, Comparison of canine and non-human primate animal models for periodontal regenerative therapy: results following a single administration of PDGF/IGF-I. J Periodontol, 65(12),1158–68.

[36] Sculean, A., Karring, T., Theilade, J., Lioubavina, N., 1997, The regenerative potential of oxytalanfibers. an experimental study in the monkey. J Clin Periodontol, 24(12),932–6.

[37] Kostopoulos, L., Karring, T., 2004, Susceptibility of GTR-regenerated periodontal attachment to ligature-induced periodontitis. J Clin Periodontol, 31(5), 336–40.

[38] Karatzas, S., Zavras, A., Greenspan, D., Amar, S., 1999, Histologic observations of periodontal wound healing after treatment with perioglas in nonhuman primates. Int J Periodontics Rest Dent, 19(5),489–99.

[39] Donos, N., Sculean, A., Glavind, L., Reich, E., Karring, T., 2003, Wound healing of degree III furcation involvements following guided tissue regeneration and/or Emdogaina histologic study. J Clin Periodontol, 30(12),1061–8.

[40] Trejo, P.M., Bonaventura, G., Weng, D., Caffesse, RG., Bragger, U., Lang, N.P., 2006, Effect of mechanical and antiseptic therapy on peri-implant mucositis: an experimental study in monkey. Clin Oral Implants Res, 17(3),294–304.

[41] Sculean, A., Donos, N., Brecx, M., Reich, E., Karring, T.,2000, Treatment of intrabony defects with guided tissue regeneration and enamel-matrix-proteins an experimental study in monkeys. J Clin Periodontol, 27(7), 466–72.

[42] Pieri, FA., Souza, M.C., Vermelho, L.L., Vermelho, ML., Perciano, P.G., Vargas, F.S., Borges, A.P., da Veiga-Junior, V.F., Moreira, M.A., 2011, Use of β-caryophyllene to combat bacterial dental plaque formation in dogs. BMC Veterinary Research, 12(1),1-8.

[43] Yimam, M., Brownell, L., Do, S.G., Lee, Y.C., Kim, D.S., Seo, K., Jeong, M., Kim, S., Jia, Q., 2019, Protective effect of UP446 on ligature-induced periodontitis in beagle dogs. Dentistry Journal, 7(2),33.

[44] Hamp, S.E., Hamp, M., Olsson, S.E., Lindberg, R., Schauman, P.,1997, Radiography of spontaneous periodontitis in dogs. J Periodontal Res, 32(7), 589–97.

[45] Haney, J.M., Zimmerman, G.J., Wikesjo, U.M., 1995, Periodontal repair in dogs: evaluation of the natural disease model. J Clin Periodontol, 22(3), 208–13.

[46] Miranda, L.A., Gomes, S.C., Soares, I.J., Oppermann, R.V., 2006, A resin-modified glass ionomer cement barrier for treating degree II furcation defects: a pilot study in dogs. Acta Odontol Scand, 64(1),37–41.

[47] Schwarz, F., Herten, M., Sager, M., Bieling, K., Sculean, A., Becker, J., 2007, Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs. Clin Oral Implants Res 18(2),161–70.

[48] Lin, P., Niimi, H., Ohsugi, Y., Tsuchiya, Y., Shimohira, T., Komatsu, K., Liu, A., Shiba, T., Aoki, A., Iwata, T., Katagiri, S., 2021, Application of Ligature-Induced Periodontitis in Mice to Explore the Molecular Mechanism of Periodontal Disease. International Journal of Molecular Sciences, 22(16), 8900.

[49] Jacob, S.P, Nath, S., 2013, Rat gingival model for testing drugs influencing inflammation. IeJSME, 7(2),8-16.

[50] Huang, K.K., Shen, C., Chiang, C.Y., Hsieh, Y.D., Fu, E., 2005, Effects of bone morphogenetic protein-6 on periodontal wound healing in a fenestration defect of rats. J Periodontal Res, 40(1),1–10.

[51] Eslami, B., Behnia, H., Javadi, H., Khiabani, K.S., Saffar, A.S., 2003, Histopathologic comparison of normal and hyperplastic condyles. Oral Surg Oral Med Oral Pathol Oral RadiolEndod, 96(6),711–7.

[52] Graves, D.T., Fine, D., Teng, Y.T., Van, Dyke., T.E., Hajishengallis, G., 2008, The use of rodent models to investigate host–bacteria interactions related to periodontal diseases. Journal of clinical periodontology, 35(2), 89-105.

[53] Lallam-Laroye, C., Escartin, Q., Zlowodzki, A.S., et al., 2006, A. Periodontitis destructions are restored by synthetic glycosaminoglycan mimetic. J Biomed Mater Res, 79(3), 675–83.

[54] Baron, R., Saffar, J.L., 1978, A quantitative study of bone remodeling during experimental periodontal disease in the golden hamster. J Periodontal Res, 13(4), 309–15.

[55] Thumbigere, Math., V, Rebouças., P, Giovani., P.A., Puppin-Rontani, R.M., Casarin, R., Martins, L., Wang, L., Krzewski, K., Introne, W.J., Somerman, M.J., Nociti, Jr., FH., 2018, Periodontitis in Chédiak-Higashi syndrome: An altered immunoinflammatory response. JDR clinical & translational research, 3(1), 35-46.

[56] Hammer, A.S., Andersen, T.H., Eriksen, T., Kortegaard, H.E., Dietz, H.H., Chriél, M., 2005, Radiographic evaluation of destructive periodontal disease in blue mink in relation to age and blood morphology. Canadian journal of veterinary research, 69(2),128.

[57] Johnson-Delaney, C.A., 2016, Exotic Animal Practice. Anatomy and disorders of the oral cavity of ferrets and other exotic companion carnivores. Veterinary Clinics,19(3),901-28.

[58] Harper, D.S, Mann, P.H., Regnier S., 1990, Measurement of dietary and dentifrice effects upon calculus accumulation rates in the domestic ferret. J Dent Res, 69,447-50.

[59] Weinberg, M.A., Bral, M., 1999, Periodontol Laboratory animal models in periodontology. J Clin, 26(6), 335–40.

[60] Tyrrell, K.L., Citron, D.M., Jenkins, J.R, Goldstein, E.J., Periodontal bacteria in rabbit mandibular and maxillary abscesses. J Clin Microbiol, 40, 1044-7.

[61] Oortgiesen, D.A., Meijer, G.J., Bronckers, A.L., Walboomers, X.F., Jansen, J.A., 2010, Fenestration defects in the rabbit jaw: An inadequate model for studying periodontal regeneration. Tissue Eng Part C Methods, 16, 133-40.

[62] Priyanka, M., Ramamurthy, J., 2015, Tissue engineering in periodontal regeneration. Res J Pharm Bio Chem Sci, 69,78-82.

[63] Ranganatha, N., Kuppast, I.J., 2012, A review on alternatives to animal testing methods in drug development. Int J Pharm Pharm Bio Sci, 4,28-32.

[64] Holmes, M., Thomas, R., Hamerow, H., 2021, Periodontal disease in sheep and cattle: Understanding dental health in past animal populations. International Journal of Paleopathology, 1(33),43-54.

[65] Wang, S., Liu, Y., Fang, D., Shi, S., 2007, The miniature pig: A useful large animal model for dental and orofacial research. Oral Dis, 13,530-7.

[66] Polejaeva, I.A., Chen, S.H., Vaught, T.D, Page, R.L, Mullins, J, Ball, S., et al., 2000, Cloned pigs produced by nuclear transfer from adult somatic cells. Nature, 407,86-90.

[67] Fawzy, El-Sayed, K.M., Dörfer, C.E., 2017, Animal Models for Periodontal Tissue Engineering: A Knowledge-Generating Process. Tissue Eng Part C Methods, 23(12), 900-925.