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Published Online: 1 December 2017

Animal Models for Periodontal Tissue Engineering: A Knowledge-Generating Process

Publication: Tissue Engineering Part C: Methods
Volume 23, Issue Number 12

Abstract

The human periodontium is a uniquely complex vital structure, supporting and anchoring the teeth in their alveolar sockets, thereby playing a decisive role in tooth homeostasis and function. Chronic periodontitis is a highly prevalent immune-inflammatory disease of the periodontium, affecting 15% of adult individuals, and is characterized by progressive destruction of the periodontal tooth-investing tissues, culminating in their irreversible damage. Current periodontal evidence-based treatment strategies achieve periodontal healing via repair processes, mostly combating the inflammatory component of the disease, to halt or reduce prospective periodontal tissue loss. However, complete periodontal tissue regeneration remains a hard fought-for goal in the field of periodontology and multiple in vitro and in vivo studies have been conducted, in the conquest to achieve a functional periodontal tissue regeneration in humans. The present review evaluates the current status of periodontal regeneration attempted through tissue-engineering concepts, ideal requirements for experimental animal models under investigation, the methods of induction and classification of the experimentally created periodontal defects, types of experimental defects employed in the diverse animal studies, as well as the current state of knowledge obtained from in vivo animal experiments, with special emphasis on large animal models.

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References

1.
Cho M.I., and Garant P.R. Development and general structure of the periodontium. Periodontology 2000 24, 9, 2000.
2.
Seo B.M., Miura M., Gronthos S., Bartold P.M., Batouli S., Brahim J., Young M., Robey P.G., Wang C.Y., and Shi S. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364, 149, 2004.
3.
Fawzy El-Sayed K.M., and Dörfer C.E. Gingival mesenchymal stem/progenitor cells: a unique tissue engineering gem. Stem Cells Int 2016, 7154327, 2016.
4.
El-Sayed K.M.F., Paris S., Becker S., Kassem N., Ungefroren H., Fandrich F., Wiltfang J., and Dorfer C. Isolation and characterization of multipotent postnatal stem/progenitor cells from human alveolar bone proper. J Cranio Maxill Surg 40, 735, 2012.
5.
Morsczeck C., Gotz W., Schierholz J., Zeilhofer F., Kuhn U., Mohl C., Sippel C., and Hoffmann K.H. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24, 155, 2005.
6.
Hughes F.J., Ghuman M., and Talal A. Periodontal regeneration: a challenge for the tissue engineer? Proc Inst Mech Eng H 224, 1345, 2010.
7.
Berlin-Broner Y., Febbraio M., and Levin L. Association between apical periodontitis and cardiovascular diseases: a systematic review of the literature. Int Endod J 50, 847, 2017.
8.
Tang Q., Fu H., Qin B., Hu Z., Liu Y., Liang Y., Zhou L., Yang Z., and Zhong R. A possible link between rheumatoid arthritis and periodontitis: a systematic review and meta-analysis. Int J Periodontics Restorative Dent 37, 79, 2017.
9.
Corbella S., Taschieri S., Del Fabbro M., Francetti L., Weinstein R., and Ferrazzi E. Adverse pregnancy outcomes and periodontitis: a systematic review and meta-analysis exploring potential association. Quintessence Int 47, 193, 2016.
10.
Pradhan S., and Goel K. Interrelationship between diabetes and periodontitis: a review. JNMA J Nepal Med Assoc 51, 144, 2011.
11.
Suzuki Y., Nakamura N., Miyabe M., Nishikawa T., Miyajima S., Adachi K., Mizutani M., Kikuchi T., Miyazawa K., Goto S., Tsukiyama K., Yamada Y., Ohno N., Noguchi T., Mitani A., Matsubara T., and Naruse K. Anti-inflammatory role of glucose-dependent insulinotropic polypeptide in periodontitis. J Diabetes Invest 7, 497, 2016.
12.
Abariga S.A., and Whitcomb B.W. Periodontitis and gestational diabetes mellitus: a systematic review and meta-analysis of observational studies. BMC Pregnancy Childbirth 16, 344, 2016.
13.
Botero J.E., Rodriguez C., and Agudelo-Suarez A.A. Periodontal treatment and glycaemic control in patients with diabetes and periodontitis: an umbrella review. Aust Dent J 61, 134, 2016.
14.
Potempa J., and Travis J. Porphyromonas gingivalis proteinases in periodontitis, a review. Acta Biochim Pol 43, 455, 1996.
15.
Cekici A., Kantarci A., Hasturk H., and Van Dyke T.E. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontology 2000 64, 57, 2014.
16.
Chapple I.L. Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodontol 24, 287, 1997.
17.
Waddington R.J., Moseley R., and Embery G. Reactive oxygen species: a potential role in the pathogenesis of periodontal diseases. Oral Dis 6, 138, 2000.
18.
Gustafsson A., and Asman B. Increased release of free oxygen radicals from peripheral neutrophils in adult periodontitis after Fc delta-receptor stimulation. J Clin Periodontol 23, 38, 1996.
19.
Darden A.G., Ries W.L., Wolf W.C., Rodriguiz R.M., and Key L.L. Jr. Osteoclastic superoxide production and bone resorption: stimulation and inhibition by modulators of NADPH oxidase. J Bone Miner Res 11, 671, 1996.
20.
Key L.L. Jr., Wolf W.C., Gundberg C.M., and Ries W.L. Superoxide and bone resorption. Bone 15, 431, 1994.
21.
McCauley L.K., and Nohutcu R.M. Mediators of periodontal osseous destruction and remodeling: principles and implications for diagnosis and therapy. J Periodontol 73, 1377, 2002.
22.
Rosier B.T., De Jager M., Zaura E., and Krom B.P. Historical and contemporary hypotheses on the development of oral diseases: are we there yet? Front Cell Infect Microbiol 4, 92, 2014.
23.
Smith P.C., Martinez C., Caceres M., and Martinez J. Research on growth factors in periodontology. Periodontology 2000 67, 234, 2015.
24.
Bartold P.M., McCulloch C.A., Narayanan A.S., and Pitaru S. Tissue engineering: a new paradigm for periodontal regeneration based on molecular and cell biology. Periodontol 2000 24, 253, 2000.
25.
Wikesjo U.M., and Selvig K.A. Periodontal wound healing and regeneration. Periodontology 2000 19, 21, 1999.
26.
Melcher A.H. On the repair potential of periodontal tissues. J Periodontol 47, 256, 1976.
27.
Ellegaard B., Karring T., and Loe H. New periodontal attachment procedure based on retardation of epithelial migration. J Clin Periodontol 1, 75, 1974.
28.
Nyman S., Karring T., Lindhe J., and Planten S. Healing following implantation of periodontitis-affected roots into gingival connective-tissue. J Clin Periodontol 7, 394, 1980.
29.
Nyman S., Gottlow J., Karring T., and Lindhe J. The regenerative potential of the periodontal ligament. An experimental study in the monkey. J Clin Periodontol 9, 257, 1982.
30.
Nyman S., Gottlow J., Lindhe J., Karring T., and Wennstrom J. New attachment formation by guided tissue regeneration. J Periodontal Res 22, 252, 1987.
31.
Gottlow J., Nyman S., Lindhe J., Karring T., and Wennstrom J. New attachment formation in the human periodontium by guided tissue regeneration. Case reports. J Clin Periodontol 13, 604, 1986.
32.
Karring T., Nyman S., Gottlow J., and Laurell L. Development of the biological concept of guided tissue regeneration—animal and human studies. Periodontology 2000 1, 26, 1993.
33.
Giannobile W.V. Periodontal tissue engineering by growth factors. Bone 19, 23S, 1996.
34.
Koop R., Merheb J., and Quirynen M. Periodontal regeneration with enamel matrix derivative (EMD) in reconstructive periodontal therapy: a systematic review. J Periodontol 83, 707, 2012.
35.
Sculean A., Nikolidakis D., and Schwarz F. Regeneration of periodontal tissues: combinations of barrier membranes and grafting materials—biological foundation and preclinical evidence: a systematic review. J Clin Periodontol 35, 106, 2008.
36.
Kao R.T., Nares S., and Reynolds M.A. Periodontal regeneration—intrabony defects: a systematic review from the AAP Regeneration Workshop. J Periodontol 86, S77, 2015.
37.
Wang H.L., Greenwell H., Fiorellini J., Giannobile W., Offenbacher S., Salkin L., Townsend C., Sheridan P., and Genco R.J. Periodontal regeneration. J Periodontol 76, 1601, 2005.
38.
Reynolds M.A., Aichelmann-Reidy M.E., Branch-Mays G.L., and Gunsolley J.C. The efficacy of bone replacement grafts in the treatment of periodontal osseous defects. A systematic review. Ann Periodontol 8, 227, 2003.
39.
Bartold P.M., Gronthos S., Ivanovski S., Fisher A., and Hutmacher D.W. Tissue engineered periodontal products. J Periodontal Res 51, 1, 2016.
40.
Carlson N.E., and Roach R.B. Jr. Platelet-rich plasma: clinical applications in dentistry. J Am Dent Assoc 133, 1383, 2002.
41.
Ivanovski S. Periodontal regeneration. Aust Dental J 54, S118, 2009.
42.
Esposito M., Grusovin M.G., Papanikolaou N., Coulthard P., and Worthington H.V. Enamel matrix derivative (Emdogain(R)) for periodontal tissue regeneration in intrabony defects. Cochrane Database Syst Rev CD003875, 2009.
43.
Needleman I.G., Worthington H.V., Giedrys-Leeper E., and Tucker R.J. Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev CD001724, 2006.
44.
Needleman I.G., Giedrys-Leeper E., Tucker R.J., and Worthington H.V. Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev CD001724, 2001.
45.
Cortellini P., Paolo G., Prato P., and Tonetti M.S. Long-term stability of clinical attachment following guided tissue regeneration and conventional therapy. J Clin Periodontol 23, 106, 1996.
46.
Trombelli L., Kim C.K., Zimmerman G.J., and Wikesjo U.M. Retrospective analysis of factors related to clinical outcome of guided tissue regeneration procedures in intrabony defects. J Clin Periodontol 24, 366, 1997.
47.
Nowzari H., and Slots J. Microorganisms in polytetrafluoroethylene barrier membranes for guided tissue regeneration. J Clin Periodontol 21, 203, 1994.
48.
Mayfield L., Soderholm G., Hallstrom H., Kullendorff B., Edwardsson S., Bratthall G., Bragger U., and Attstrom R. Guided tissue regeneration for the treatment of intraosseous defects using a biabsorbable membrane. A controlled clinical study. J Clin Periodontol 25, 585, 1998.
49.
Laurell L., Gottlow J., Zybutz M., and Persson R. Treatment of intrabony defects by different surgical procedures. A literature review. J Periodontol 69, 303, 1998.
50.
Cury P.R., Furuse C., Martins M.T., Sallum E.A., and De Araujo N.S. Root resorption and ankylosis associated with guided tissue regeneration. J Am Dent Assoc 136, 337, 2005.
51.
Blomlof L., and Lindskog S. Cervical root resorption associated with guided tissue regeneration: a case report. J Periodontol 69, 392, 1998.
52.
Park J.C., Um Y.J., Jung U.W., Kim C.S., Choi S.H., and Kim C.K. Histological characteristics of newly formed cementum in surgically created one-wall intrabony defects in a canine model. J Periodontal Implant Sci 40, 3, 2010.
53.
Bartold P.M., and Narayanan A.S. Molecular and cell biology of healthy and diseased periodontal tissues. Periodontology 2000 40, 29, 2006.
54.
Lang H., Schuler N., and Nolden R. Attachment formation following replantation of cultured cells into periodontal defects—a study in minipigs. J Dent Res 77, 393, 1998.
55.
Bilbeissi M.W., Kerebel B., and Daniel A. Treatment of a periodontal intrabony pocket in man by a mucoperiosteal free graft combined with a calcium phosphate implant. Bull Group Int Rech Sci Stomatol Odontol 32, 99, 1989.
56.
Gronthos S., Mankani M., Brahim J., Robey P.G., and Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A 97, 13625, 2000.
57.
Fawzy El-Sayed K.M., Dörfer C., Fandrich F., Gieseler F., Moustafa M.H., and Ungefroren H. Adult mesenchymal stem cells explored in the dental field. Adv Biochem Eng Biotechnol 130, 89, 2013.
58.
Miura M., Gronthos S., Zhao M., Lu B., Fisher L.W., Robey P.G., and Shi S. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100, 5807, 2003.
59.
Sonoyama W., Liu Y., Yamaza T., Tuan R.S., Wang S., Shi S., and Huang G.T. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34, 166, 2008.
60.
Sato A., Okumura K., Matsumoto S., Hattori K., Hattori S., Shinohara M., and Endo F. Isolation, tissue localization, and cellular characterization of progenitors derived from adult human salivary glands. Cloning Stem Cells 9, 191, 2007.
61.
Zhang Q., Shi S., Liu Y., Uyanne J., Shi Y., and Le A.D. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183, 7787, 2009.
62.
Yan X., Qin H., Qu C., Tuan R.S., Shi S., and Huang G.T. iPS cells reprogrammed from human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem Cells Dev 19, 469, 2010.
63.
Wada N., Wang B., Lin N.H., Laslett A.L., Gronthos S., and Bartold P.M. Induced pluripotent stem cell lines derived from human gingival fibroblasts and periodontal ligament fibroblasts. J Periodontal Res 46, 438, 2011.
64.
Miyoshi K., Tsuji D., Kudoh K., Satomura K., Muto T., Itoh K., and Noma T. Generation of human induced pluripotent stem cells from oral mucosa. J Biosci Bioeng 110, 345, 2010.
65.
Trofin E.A., Monsarrat P., and Kemoun P. Cell therapy of periodontium: from animal to human? Front Physiol 4, 325, 2013.
66.
Discher D.E., Mooney D.J., and Zandstra P.W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673, 2009.
67.
Chen F.M., and Jin Y. Periodontal tissue engineering and regeneration: current approaches and expanding opportunities. Tissue Eng Part B Rev 16, 219, 2010.
68.
Dyer B.L., Caffesse R.G., Nasjleti C.E., and Morrison E.C. Guided tissue regeneration with dentin biomodification. J Periodontol 64, 1052, 1993.
69.
Lin Z., Rios H.F., and Cochran D.L. Emerging regenerative approaches for periodontal reconstruction: a systematic review from the AAP regeneration workshop. J Periodontol 86, S134, 2015.
70.
Kaigler D., Cirelli J.A., and Giannobile W.V. Growth factor delivery for oral and periodontal tissue engineering. Expert Opin Drug Deliv 3, 647, 2006.
71.
Schilephake H. Bone growth factors in maxillofacial skeletal reconstruction. Int J Oral Maxillofac Surg 31, 469, 2002.
72.
Bosshardt D.D. Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels. J Clin Periodontol 35, 87, 2008.
73.
Moshaverinia A., Chen C., Xu X., Akiyama K., Ansari S., Zadeh H.H., and Shi S. Bone regeneration potential of stem cells derived from periodontal ligament or gingival tissue sources encapsulated in RGD-modified alginate scaffold. Tissue Eng Part A 20, 611, 2014.
74.
Garg T., Singh O., Arora S., and Murthy R. Scaffold: a novel carrier for cell and drug delivery. Crit Rev Ther Drug Carrier Syst 29, 1, 2012.
75.
Park C.H., Rios H.F., Taut A.D., Padial-Molina M., Flanagan C.L., Pilipchuk S.P., Hollister S.J., and Giannobile W.V. Image-based, fiber guiding scaffolds: a platform for regenerating tissue interfaces. Tissue Eng Part C Methods 20, 533, 2014.
76.
King G.N., King N., and Hughes F.J. Effect of two delivery systems for recombinant human bone morphogenetic protein-2 on periodontal regeneration in vivo. J Periodontal Res 33, 226, 1998.
77.
Howell T.H., Fiorellini J., Jones A., Alder M., Nummikoski P., Lazaro M., Lilly L., and Cochran D. A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation or augmentation. Int J Periodontics Restorative Dent 17, 124, 1997.
78.
Talwar R., Di Silvio L., Hughes F.J., and King G.N. Effects of carrier release kinetics on bone morphogenetic protein-2-induced periodontal regeneration in vivo. J Clin Periodontol 28, 340, 2001.
79.
Fawzy El-Sayed K.M., Dorfer C., Fandrich F., Gieseler F., Moustafa M.H., and Ungefroren H. Adult mesenchymal stem cells explored in the dental field. Adv Biochem Eng Biotechnol 130, 89, 2013.
80.
Fawzy El-Sayed K.M., Mekhemar M.K., Beck-Broichsitter B.E., Bahr T., Hegab M., Receveur J., Heneweer C., Becker S.T., Wiltfang J., and Dorfer C.E. Periodontal regeneration employing gingival margin-derived stem/progenitor cells in conjunction with IL-1ra-hydrogel synthetic extracellular matrix. J Clin Periodontol 42, 448, 2015.
81.
Fawzy El-Sayed K.M., Paris S., Becker S.T., Neuschl M., De Buhr W., Salzer S., Wulff A., Elrefai M., Darhous M.S., El-Masry M., Wiltfang J., and Dorfer C.E. Periodontal regeneration employing gingival margin-derived stem/progenitor cells: an animal study. J Clin Periodontol 39, 861, 2012.
82.
Liu Y., Zheng Y., Ding G., Fang D., Zhang C., Bartold P.M., Gronthos S., Shi S., and Wang S. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 26, 1065, 2008.
83.
Fawzy El-Sayed K.M., Dahaba M.A., Aboul-Ela S., and Darhous M.S. Local application of hyaluronan gel in conjunction with periodontal surgery: a randomized controlled trial. Clin Oral Investig 16, 1229, 2012.
84.
Li H., Yang H., Ding Y., Aprecio R., Zhang W., Wang Q., and Li Y. Experimental periodontitis induced by Porphyromonas gingivalis does not alter the onset or severity of diabetes in mice. J Periodontal Res 48, 582, 2013.
85.
Grauballe M.B., Ostergaard J.A., Schou S., Flyvbjerg A., and Holmstrup P. Blockade of RAGE in Zucker obese rats with experimental periodontitis. J Periodontal Res 52, 97, 2017.
86.
Xu R., Zeng G., Wang S.Y., Tao H., Ren L., Zhang Z., Zhang Q.N., Zhao J.X., Gao J., and Li D.X. Periodontitis promotes the diabetic development of obese rat via miR-147 induced classical macrophage activation. Biomed Pharmacother 83, 892, 2016.
87.
Kose O., Arabaci T., Gedikli S., Eminoglu D.O., Kermen E., Kizildag A., Kara A., Ozkanlar S., and Yemenoglu H. Biochemical and histopathologic analysis of the effects of periodontitis on left ventricular heart tissues of rats. J Periodontal Res 52, 176, 2017.
88.
Kose O., Arabaci T., Yemenoglu H., Ozkanlar S., Kurt N., Gumussoy I., Gedikli S., and Kara A. Influence of experimental periodontitis on cardiac oxidative stress in rats: a biochemical and histomorphometric study. J Periodontal Res 52, 603, 2017.
89.
Funaki S., Tokutomi F., Wada-Takahashi S., Yoshino F., Yoshida A., Maehata Y., Miyamoto C., Toyama T., Sato T., Hamada N., Lee M.C.I., and Takahashi S.S. Porphyromonas gingivalis infection modifies oral microcirculation and aortic vascular function in the stroke-prone spontaneously hypertensive rat (SHRSP). Microb Pathog 92, 36, 2016.
90.
Sandal I., Karydis A., Luo J., Prislovsky A., Whittington K.B., Rosloniec E.F., Dong C., Novack D.V., Mydel P., Zheng S.G., Radic M.Z., and Brand D.D. Bone loss and aggravated autoimmune arthritis in HLA-DRbeta1-bearing humanized mice following oral challenge with Porphyromonas gingivalis. Arthritis Res Therapy 18, 249, 2016.
91.
Oz H.S., and Puleo D.A. Animal models for periodontal disease. J Biomed Biotechnol 2011, 754857, 2011.
92.
Dannan A., and Alkattan F. Animal models in periodontal research: a mini-review of the literature. Int J Vet Med 5, 1, 2008.
93.
Fine D.H. Of mice and men: animal models of human periodontal disease. J Clin Periodontol 36, 913, 2009.
94.
Weinberg M.A., and Bral M. Laboratory animal models in periodontology. J Clin Periodontol 26, 335, 1999.
95.
Hamp S.E., Lindhe J., and Loe H. Experimental periodontitis in the beagle dog. J Periodontal Res 10, 13, 1972.
96.
Baker D.L., and Seymour G.J. The possible pathogenesis of gingival recession. A histological study of induced recession in the rat. J Clin Periodontol 3, 208, 1976.
97.
Ericsson I., and Lindhe J. Lack of effect of trauma from occlusion on the recurrence of experimental periodontitis. J Clin Periodontol 4, 115, 1977.
98.
Kantarci A., Hasturk H., and Van Dyke T.E. Animal models for periodontal regeneration and peri-implant responses. Periodontology 2000 68, 66, 2015.
99.
Hughes H.C. Jr., and Lang C.M. Basic principles in selecting animal species for research projects. Clin Toxicol 13, 611, 1978.
100.
Lang H., Schuler N., Arnhold S., Nolden R., and Mertens T. Formation of differentiated tissues in-vivo by periodontal cell-populations cultured in-vitro. J Dent Res 74, 1219, 1995.
101.
Lindhe J., Pontoriero R., Berglundh T., and Araujo M. The effect of flap management and bioresorbable occlusive devices in GTR treatment of degree III furcation defects. An experimental study in dogs. J Clin Periodontol 22, 276, 1995.
102.
Blomlof J., Jansson L., Blomlof L., and Lindskog S. Root surface etching at neutral pH promotes periodontal healing. J Clin Periodontol 23, 50, 1996.
103.
Weng D., Hurzeler M.B., Quinones C.R., Pechstadt B., Mota L., and Caffesse R.G. Healing patterns in recession defects treated with ePTFE membranes and with free connective tissue grafts. A histologic and histometric study in the beagle dog. J Clin Periodontol 25, 238, 1998.
104.
Schou S., Holmstrup P., and Kornman K.S. Non-human primates used in studies of periodontal disease pathogenesis: a review of the literature. J Periodontol 64, 497, 1993.
105.
Giannobile W.V., Finkelman R.D., and Lynch S.E. 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, 1158, 1994.
106.
Sugaya A., Minabe M., Hori T., Tatsumi J., Watanabe Y., Ikeda K., Numabe Y., Hayashi H., and Kamoi K. Effects on wound-healing of tricalcium phosphate-collagen complex implants in periodontal osseous defects in the dog. J Periodontal Res 25, 60, 1990.
107.
Madden T.E., and Caton J.G. Animal models for periodontal disease. Methods Enzymol 235, 106, 1994.
108.
Fischer R.G., and Klinge B. Clinical and histological evaluation of ligature-induced periodontitis in the domestic ferret. J Clin Periodontol 21, 230, 1994.
109.
Kimura S., Nagai A., Onitsuka T., Koga T., Fujiwara T., Kaya H., and Hamada S. Induction of experimental periodontitis in mice with Porphyromonas gingivalis-adhered ligatures. J Periodontol 71, 1167, 2000.
110.
Hojo K., Tamura A., Mizoguchi C., Kato D., Ohshima T., and Maeda N. Predominant bacteria recovered from a periodontitis site in a hamster model raised by silk-ligature with Prophyromonas gingivalis infection. Biosci Biotechnol Biochem 72, 1348, 2008.
111.
Genco C.A., Van Dyke T., and Amar S. Animal models for Porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 6, 444, 1998.
112.
Polak D., Wilensky A., Shapira L., Halabi A., Goldstein D., Weiss E.I., and Houri-Haddad Y. Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: bone loss and host response. J Clin Periodontol 36, 406, 2009.
113.
Gangula P., Ravella K., Chukkapalli S., Rivera M., Srinivasan S., Hale A., Channon K., Southerland J., and Kesavalu L. Polybacterial periodontal pathogens alter vascular and gut BH4/nNOS/NRF2-phase II enzyme expression. PLoS One 10, e0129885, 2015.
114.
Li Y., Lu Z., Zhang X., Yu H., Kirkwood K.L., Lopes-Virella M.F., and Huang Y. Metabolic syndrome exacerbates inflammation and bone loss in periodontitis. J Dent Res 94, 362, 2015.
115.
Shklar G. Periodontal disease in experimental animals subjected to chronic cold stress. J Periodontol 37, 377, 1966.
116.
Lu H., Xu M., Wang F., Liu S., Gu J., Lin S., and Zhao L. Chronic stress accelerates ligature-induced periodontitis by suppressing glucocorticoid receptor-alpha signaling. Exp Mol Med 48, e223, 2016.
117.
Graves D.T., Fine D., Teng Y.T.A., Van Dyke T.E., and Hajishengallis G. The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 35, 89, 2008.
118.
Leone C.W., Bokhadhoor H., Kuo D., Desta T., Yang J., Siqueira M.F., Amar S., and Graves D.T. Immunization enhances inflammation and tissue destruction in response to Porphyromonas gingivalis. Infect Immun 74, 2286, 2006.
119.
Amar S., Wu S., and Madan M. Is Porphyromonas gingivalis cell invasion required for atherogenesis? Pharmacotherapeutic implications. J Immunol 182, 1584, 2009.
120.
Maekawa T., Takahashi N., Tabeta K., Aoki Y., Miyashita H., Miyauchi S., Miyazawa H., Nakajima T., and Yamazaki K. Chronic oral infection with Porphyromonas gingivalis accelerates atheroma formation by shifting the lipid profile. PLoS One 6, e20240, 2011.
121.
Ophir G., Amariglio N., Jacob-Hirsch J., Elkon R., Rechavi G., and Michaelson D.M. Apolipoprotein E4 enhances brain inflammation by modulation of the NF-kappa B signaling cascade. Neurobiol Dis 20, 709, 2005.
122.
Yao X.L., Fredriksson K., Yu Z.X., Xu X.L., Raghavachari N., Keeran K.J., Zywicke G.J., Kwak M., Amar M.J.A., Remaley A.T., and Levine S.J. Apolipoprotein E negatively regulates house dust mite-induced asthma via a low-density lipoprotein receptor-mediated pathway. Am J Resp Crit Care 182, 1228, 2010.
123.
Zhang T., Kurita-Ochiai T., Hashizume T., Du Y.A., Oguchi S., and Yamamoto M. Aggregatibacter actinomycetemcomitans accelerates atherosclerosis with an increase in atherogenic factors in spontaneously hyperlipidemic mice. Fems Immunol Med Mic 59, 143, 2010.
124.
Mkonyi L.E., Bakken V., Sovik J.B., Mauland E.K., Fristad I., Barczyk M.M., Bletsa A., and Berggreen E. Lymphangiogenesis is induced during development of periodontal disease. J Dent Res 91, 71, 2012.
125.
Gyurko R., Siqueira C.C., Caldon N., Gao L., Kantarci A., and Van Dyke T.E. Chronic hyperglycemia predisposes to exaggerated inflammatory response and leukocyte dysfunction in Akita mice. J Immunol 177, 7250, 2006.
126.
Li C.H., and Amar S. Morphometric, histomorphometric, and microcomputed tomographic analysis of periodontal inflammatory lesions in a murine model. J Periodontol 78, 1120, 2007.
127.
Harper D.S., Mann P.H., and Regnier S. Measurement of dietary and dentifrice effects upon calculus accumulation rates in the domestic ferret. J Dent Res 69, 447, 1990.
128.
Zhao M., Jin Q., Berry J.E., Nociti F.H. Jr., Giannobile W.V., and Somerman M.J. Cementoblast delivery for periodontal tissue engineering. J Periodontol 75, 154, 2004.
129.
Goncalves F., de Moraes M.S., Ferreira L.B., Carreira A.C.O., Kossugue P.M., Boaro L.C.C., Bentini R., Garcia C.R.D., Sogayar M.C., Arana-Chavez V.E., and Catalani L.H. Combination of bioactive polymeric membranes and stem cells for periodontal regeneration: in vitro and in vivo analyses. PLoS One 11, e0152412, 2016.
130.
Yu X., Lv L., Zhang J., Zhang T., Xiao C., and Li S. Expression of neuropeptides and bone remodeling-related factors during periodontal tissue regeneration in denervated rats. J Mol Histol 46, 195, 2015.
131.
Liu H., Li M., Du L., Yang P., and Ge S. Local administration of stromal cell-derived factor-1 promotes stem cell recruitment and bone regeneration in a rat periodontal bone defect model. Mater Sci Eng C Mater Biol Appl 53, 83, 2015.
132.
Nakajima D., Tabata Y., and Sato S. Periodontal tissue regeneration with PRP incorporated gelatin hydrogel sponges. Biomed Mater 10, 055016, 2015.
133.
Dundar S., Eltas A., Hakki S.S., Malkoc S., Uslu M.O., Tuzcu M., Komorowski J., Ozercan I.H., Akdemir F., and Sahin K. Dietary arginine silicate inositol complex inhibits periodontal tissue loss in rats with ligature-induced periodontitis. Drug Des Devel Ther 10, 3771, 2016.
134.
Lisboa M.R., Gondim D.V., Ervolino E., Vale M.L., Frota N.P., Nunes N.L., Mariguela V.C., Taba M. Jr., Messora M.R., and Furlaneto F.A. Effects of electroacupuncture on experimental periodontitis in rats. J Periodontol 86, 801, 2015.
135.
Xu X.C., Chen H., Zhang X., Zhai Z.J., Liu X.Q., Zheng X.Y., Zhang J., Qin A., and Lu E.Y. Effects of oestrogen deficiency on the alveolar bone of rats with experimental periodontitis. Mol Med Rep 12, 3494, 2015.
136.
Fu M.M., Fu E., Kuo P.J., Tu H.P., Chin Y.T., Chiang C.Y., and Chiu H.C. Gelatinases and extracellular matrix metalloproteinase inducer are associated with cyclosporin-A-induced attenuation of periodontal degradation in rats. J Periodontol 86, 82, 2015.
137.
Choi E.Y., Bae S.H., Ha M.H., Choe S.H., Hyeon J.Y., Choi J.I., Choi I.S., and Kim S.J. Genistein suppresses Prevotella intermedia lipopolysaccharide-induced inflammatory response in macrophages and attenuates alveolar bone loss in ligature-induced periodontitis. Arch Oral Biol 62, 70, 2016.
138.
Dai J., Ma Y., Shi M., Cao Z., Zhang Y., and Miron R.J. Initial changes in alveolar bone volume for sham-operated and ovariectomized rats in ligature-induced experimental periodontitis. Clin Oral Investig 20, 581, 2016.
139.
Zhuang D., Ji Z., Bi L., Wang X., Zhou Q., and Cao W. Low-Intensity Ultrasound combined with hematoporphyrin monomethyl ether in the treatment of experimental periodontitis in rats. Biomed Res Int 2016, 7156716, 2016.
140.
Dong Y., Huihui Z., and Li C. Piperine inhibit inflammation, alveolar bone loss and collagen fibers breakdown in a rat periodontitis model. J Periodontal Res 50, 758, 2015.
141.
Yang X., Zhang H., Wang J., Zhang Z., and Li C. Puerarin decreases bone loss and collagen destruction in rats with ligature-induced periodontitis. J Periodontal Res 50, 748, 2015.
142.
Bhattarai G., Poudel S.B., Kook S.H., and Lee J.C. Resveratrol prevents alveolar bone loss in an experimental rat model of periodontitis. Acta Biomater 29, 398, 2016.
143.
Hatipoglu M., Saglam M., Koseoglu S., Koksal E., Keles A., and Esen H.H. The Effectiveness of Crataegus orientalis M Bieber. (Hawthorn) extract administration in preventing alveolar bone loss in rats with experimental periodontitis. PLoS One 10, e0128134, 2015.
144.
Park S.I., Kang S.J., Han C.H., Kim J.W., Song C.H., Lee S.N., Ku S.K., and Lee Y.J. The effects of topical application of polycal (a 2:98 (g/g) mixture of polycan and calcium gluconate) on experimental periodontitis and alveolar bone loss in rats. Molecules 21, 527, 2016.
145.
Arabaci T., Kermen E., Ozkanlar S., Kose O., Kara A., Kizildag A., Duman S.B., and Ibisoglu E. Therapeutic effects of melatonin on alveolar bone resorption after experimental periodontitis in rats: a biochemical and immunohistochemical study. J Periodontol 86, 874, 2015.
146.
Cai X.J., Yang F., Yan X.Z., Yang W.X., Yu N., Oortgiesen D.A.W., Wang Y.N., Jansen J.A., and Walboomers X.F. Influence of bone marrow-derived mesenchymal stem cells pre-implantation differentiation approach on periodontal regeneration in vivo. J Clin Periodontol 42, 380, 2015.
147.
Hasturk H., Goguet-Surmenian E., Blackwood A., Andry C., and Kantarci A. 1-Tetradecanol complex: therapeutic actions in experimental periodontitis. J Periodontol 80, 1103, 2009.
148.
Hasturk H., Jones V.L., Andry C., and Kantarci A. 1-Tetradecanol complex reduces progression of Porphyromonas gingivalis-induced experimental periodontitis in rabbits. J Periodontol 78, 924, 2007.
149.
Hasturk H., Kantarci A., Ebrahimi N., Andry C., Holick M., Jones V.L., and Van Dyke T.E. Topical H2 antagonist prevents periodontitis in a rabbit model. Infect Immun 74, 2402, 2006.
150.
Hasturk H., Kantarci A., Ohira T., Arita M., Ebrahimi N., Chiang N., Petasis N.A., Levy B.D., Serhan C.N., and Van Dyke T.E. RvE1 protects from local inflammation and osteoclast-mediated bone destruction in periodontitis. FASEB J 20, 401, 2006.
151.
Jain A., Batista E.L., Serhan C., Stahl G.L., and Van Dyke T.E. Role for periodontitis in the progression of lipid deposition in an animal model. Infect Immun 71, 6012, 2003.
152.
Su F., Liu S.S., Ma J.L., Wang D.S., E, L.L., and Liu H.C. Enhancement of periodontal tissue regeneration by transplantation of osteoprotegerin-engineered periodontal ligament stem cells. Stem Cell Res Ther 6, 22, 2015.
153.
Schectman L.R., Ammons W.F., Simpson D.M., and Page R.C. Host tissue response in chronic periodontal disease. 2. Histologic features of the normal periodontium, and histologic and ultrastructural manifestations of disease in the marmoset. J Periodontal Res 7, 195, 1972.
154.
Miller D.R., Aufdemorte T.B., Fox W.C., Waldrop T.C., Mealey B.L., and Brunsvold M.A. Periodontitis in the baboon—a potential model for human-disease. J Periodontal Res 30, 404, 1995.
155.
Kornman K.S., Holt S.C., and Robertson P.B. The microbiology of ligature-induced periodontitis in the cynomolgus monkey. J Periodontal Res 16, 363, 1981.
156.
Adams R.A., Zander H.A., and Polson A.M. Interproximal and buccal cell-populations apical to the sulcus before and during experimental periodontitis in squirrel-monkeys. J Periodontol 52, 416, 1981.
157.
Ebersole J.L., Brunsvold M., Steffensen B., Wood R., and Holt S.C. Effects of immunization with Porphyromonas gingivalis and Prevotella intermedia on progression of ligature-induced periodontitis in the nonhuman primate Macaca fascicularis. Infect Immun 59, 3351, 1991.
158.
Holt S.C., Ebersole J., Felton J., Brunsvold M., and Kornman K.S. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239, 55, 1988.
159.
Caton J., Mota L., Gandini L., and Laskaris B. Non-human primate models for testing the efficacy and safety of periodontal regeneration procedures. J Periodontol 65, 1143, 1994.
160.
Caton J., and Nyman S. Histometric evaluation of periodontal surgery. I. The modified Widman flap procedure. J Clin Periodontol 7, 212, 1980.
161.
Caton J., and Nyman S. Histometric evaluation of periodontal surgery. III. The effect of bone resection on the connective tissue attachment level. J Periodontol 52, 405, 1981.
162.
Caton J., Nyman S., and Zander H. Histometric evaluation of periodontal surgery. II. Connective tissue attachment levels after four regenerative procedures. J Clin Periodontol 7, 224, 1980.
163.
Caton J.G., DeFuria E.L., Polson A.M., and Nyman S. Periodontal regeneration via selective cell repopulation. J Periodontol 58, 546, 1987.
164.
Iglhaut J., Aukhil I., Simpson D.M., Johnston M.C., and Koch G. Progenitor cell kinetics during guided tissue regeneration in experimental periodontal wounds. J Periodontal Res 23, 107, 1988.
165.
Ling L.J., Lai Y.H., Hwang H., and Chen H. Response of regenerative tissues to plaque: a histological study in monkeys. J Periodontol 65, 781, 1994.
166.
Butler J.R., Rajnay Z.W., Vernino A.R., and Parker D. Volumetric changes following barrier regeneration procedures for the surgical management of grade II molar furcation defects in baboons: II. Bone, cementum, epithelium, and connective tissue. Int J Periodontics Restorative Dent 18, 58, 1998.
167.
Blumenthal N.M., Alves M.E., Al-Huwais S., Hofbauer A.M., and Koperski R.D. Defect-determined regenerative options for treating periodontal intrabony defects in baboons. J Periodontol 74, 10, 2003.
168.
Polson A.M., and Proye M.P. Fibrin linkage: a precursor for new attachment. J Periodontol 54, 141, 1983.
169.
Murakami S., Takayama S., Ikezawa K., Shimabukuro Y., Kitamura M., Nozaki T., Terashima A., Asano T., and Okada H. Regeneration of periodontal tissues by basic fibroblast growth factor. J Periodontal Res 34, 425, 1999.
170.
Takayama S., Murakami S., Shimabukuro Y., Kitamura M., and Okada H. Periodontal regeneration by FGF-2 (bFGF) in primate models. J Dent Res 80, 2075, 2001.
171.
Kato S., Kawabata N., Suzuki N., Ohmura M., and Takagi M. Bone morphogenetic protein-2 induces the differentiation of a mesenchymal progenitor cell line, ROB-C26, into mature osteoblasts and adipocytes. Life Sci 84, 302, 2009.
172.
Rawadi G., Vayssiere B., Dunn F., Baron R., and Roman-Roman S. BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J Bone Miner Res 18, 1842, 2003.
173.
Katagiri T., Yamaguchi A., Ikeda T., Yoshiki S., Wozney J.M., Rosen V., Wang E.A., Tanaka H., Omura S., and Suda T. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commun 172, 295, 1990.
174.
Fawzy El-Sayed K.M., Dörfer C., Ungefroren H., Kassem N., Wiltfang J., and Paris S. Effect of Emdogain enamel matrix derivative and BMP-2 on the gene expression and mineralized nodule formation of alveolar bone proper-derived stem/progenitor cells. J Craniomaxillofac Surg 42, 568, 2014.
175.
Wang E.A., Rosen V., D'Alessandro J.S., Bauduy M., Cordes P., Harada T., Israel D.I., Hewick R.M., Kerns K.M., LaPan P., et al. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci U S A 87, 2220, 1990.
176.
Thies R.S., Bauduy M., Ashton B.A., Kurtzberg L., Wozney J.M., and Rosen V. Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 130, 1318, 1992.
177.
Rickard D.J., Sullivan T.A., Shenker B.J., Leboy P.S., and Kazhdan I. Induction of rapid osteoblast differentiation in rat bone marrow stromal cell cultures by dexamethasone and BMP-2. Dev Biol 161, 218, 1994.
178.
Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., Rosen V., Wozney J.M., Fujisawa-Sehara A., and Suda T. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127, 1755, 1994.
179.
Notodihardjo F.Z., Kakudo N., Kushida S., Suzuki K., and Kusumoto K. Bone regeneration with BMP-2 and hydroxyapatite in critical-size calvarial defects in rats. J Craniomaxillofac Surg 40, 287, 2012.
180.
Ripamonti U., Heliotis M., Vandenheever B., and Reddi A.H. Bone Morphogenetic proteins induce periodontal regeneration in the baboon (Papio-ursinus). J Periodontal Res 29, 439, 1994.
181.
Teare J.A., Ramoshebi L.N., and Ripamonti U. Periodontal tissue regeneration by recombinant human transforming growth factor-beta 3 in Papio ursinus. J Periodontal Res 43, 1, 2008.
182.
Robinson C., Brookes S.J., Shore R.C., and Kirkham J. The developing enamel matrix: nature and function. Eur J Oral Sci 106, 282, 1998.
183.
Hammarstrom L., Heijl L., and Gestrelius S. Periodontal regeneration in a buccal dehiscence model in monkeys after application of enamel matrix proteins. J Clin Periodontol 24, 669, 1997.
184.
Van der Pauw M.T., Van den Bos T., Everts V., and Beertsen W. Enamel matrix-derived protein stimulates attachment of periodontal ligament fibroblasts and enhances alkaline phosphatase activity and transforming growth factor beta1 release of periodontal ligament and gingival fibroblasts. J Periodontol 71, 31, 2000.
185.
Gestrelius S., Andersson C., Lidstrom D., Hammarstrom L., and Somerman M. In vitro studies on periodontal ligament cells and enamel matrix derivative. J Clin Periodontol 24, 685, 1997.
186.
Hakki S.S., Berry J.E., and Somerman M.J. The effect of enamel matrix protein derivative on follicle cells in vitro. J Periodontol 72, 679, 2001.
187.
Sculean A., Junker R., Donos N., Berakdar M., Brecx M., and Dunker N. Immunohistochemical evaluation of matrix molecules associated with wound healing following regenerative periodontal treatment in monkeys. Clin Oral Investig 6, 175, 2002.
188.
Cochran D.L., Jones A., Heijl L., Mellonig J.T., Schoolfield J., and King G.N. Periodontal regeneration with a combination of enamel matrix proteins and autogenous bone grafting. J Periodontol 74, 1269, 2003.
189.
Wikesjo U.M., Kean C.J., and Zimmerman G.J. Periodontal repair in dogs: supraalveolar defect models for evaluation of safety and efficacy of periodontal reconstructive therapy. J Periodontol 65, 1151, 1994.
190.
Haney J.M., Zimmerman G.J., and Wikesjo U.M. Periodontal repair in dogs: evaluation of the natural disease model. J Clin Periodontol 22, 208, 1995.
191.
Albuquerque C., Morinha F., Requicha J., Martins T., Dias I., Guedes-Pinto H., Bastos E., and Viegas C. Canine periodontitis: the dog as an important model for periodontal studies. Vet J 191, 299, 2012.
192.
Koo K.T., Polimeni G., Albandar J.M., and Wikesjo U.M.E. Periodontal repair in dogs: examiner reproducibility in the supraalveolar periodontal defect model. J Clin Periodontol 31, 439, 2004.
193.
Kortegaard H.E., Eriksen T., and Baelum V. Periodontal disease in research beagle dogs—an epidemiological study. J Small Anim Pract 49, 610, 2008.
194.
Lindhe J., Hamp S.E., and Loe H. Plaque induced periodontal-disease in beagle dogs. A 4-year clinical, roentgenographical and histometrical study. J Periodontal Res 10, 243, 1975.
195.
Wikesjo U.M.E., and Nilveus R. Periodontal repair in dogs—healing patterns in large circumferential periodontal defects. J Clin Periodontol 18, 49, 1991.
196.
Pavlica Z., Petelin M., Nemec A., Erzen D., and Skaleric U. Measurement of total antioxidant capacity in gingival crevicular fluid and serum in dogs with periodontal disease. Am J Vet Res 65, 1584, 2004.
197.
Page R.C., and Schroeder H.E. Spontaneous chronic periodontitis in adult dogs. A clinical and histopathological survey. J Periodontol 52, 60, 1981.
198.
Sorensen W.P., Loe H., and Ramfjord S.P. Periodontal disease in the beagle dog. A cross sectional clinical study. J Periodontal Res 15, 380, 1980.
199.
Struillou X., Boutigny H., Soueidan A., and Layrolle P. Experimental animal models in periodontology: a review. Open Dent J 4, 37, 2010.
200.
Lindhe J., Hamp S.E., and Loe H. Experimental periodontitis in the beagle dog. Int Dent J 23, 432, 1973.
201.
Matsuura M., Herr Y., Han K.Y., Lin W.L., Genco R.J., and Cho M.I. Immunohistochemical expression of extracellular matrix components of normal and healing periodontal tissues in the beagle dog. J Periodontol 66, 579, 1995.
202.
Kwon D.H., Bennett W., Herberg S., Bastone P., Pippig S., Rodriguez N.A., Susin C., and Wikesjo U.M. Evaluation of an injectable rhGDF-5/PLGA construct for minimally invasive periodontal regenerative procedures: a histological study in the dog. J Clin Periodontol 37, 390, 2010.
203.
Egelberg J. Local effect of diet on plaque formation and development of gingivitis in dogs. 3. Effect of frequency of meals and tube feeding. Odontolo Revy 16, 50, 1965.
204.
Carlsson J., and Egelberg J. Local effect of diet on plaque formation and development of gingivitis in dogs. II. Effect of high carbohydrate versus high protein-fat diets. Odontol Revy 16, 42, 1965.
205.
Egelberg J. Local effect of diet on plaque formation and development of gingivitis in dogs. I. Effect of hard and soft diets. Odontol Revy 16, 31, 1965.
206.
Holland M., Boring J.G., Boyle C.R., Pickrum H.M., and Jeffcoat M.K. Radiographic bone loss correlations and technetium-99m-MDP bone uptake in ligature-induced periodontal disease in the beagle. Vet Radiol Ultrasound 39, 366, 1998.
207.
Kim C.S., Choi S.H., Chai J.K., Cho K.S., Moon I.S., Wikesjo U.M., and Kim C.K. Periodontal repair in surgically created intrabony defects in dogs: influence of the number of bone walls on healing response. J Periodontol 75, 229, 2004.
208.
Tal H., Pitaru S., Moses O., and Kozlovsky A. Collagen gel and membrane in guided tissue regeneration in periodontal fenestration defects in dogs. J Clin Periodontol 23, 1, 1996.
209.
Boyko G.A., Melcher A.H., and Brunette D.M. Formation of new periodontal ligament by periodontal ligament cells implanted in vivo after culture in vitro. A preliminary study of transplanted roots in the dog. J Periodontal Res 16, 73, 1981.
210.
Levy P., Nevins A., and Laporta R. Healing potential of surgically-induced periodontal osseous defects in animals using mineralized collagen gel xenografts. J Periodontol 52, 303, 1981.
211.
Sugaya A., Minabe M., Tamura T., Hori T., and Watanabe Y. Effects on wound-healing of hydroxyapatite-collagen complex implants in periodontal osseous defects in the dog. J Periodontal Res 24, 284, 1989.
212.
Plotzke A.E., Barbosa S., Nasjleti C.E., Morrison E.C., and Caffesse R.G. Histologic and histometric responses to polymeric composite grafts. J Periodontol 64, 343, 1993.
213.
Zang S., Dong G., Peng B., Xu J., Ma Z., Wang X., Liu L., and Wang Q. A comparison of physicochemical properties of sterilized chitosan hydrogel and its applicability in a canine model of periodontal regeneration. Carbohydrate Polym 113, 240, 2014.
214.
Aukhil I., Simpson D.M., Suggs C., and Pettersson E. In vivo differentiation of progenitor cells of the periodontal ligament. An experimental study using physical barriers. J Clin Periodontol 13, 862, 1986.
215.
Aukhil I., Simpson D.M., and Schaberg T.V. An experimental study of new attachment procedure in beagle dogs. J Periodontal Res 18, 643, 1983.
216.
Aukhil I., Pettersson E., and Suggs C. Guided tissue regeneration. An experimental procedure in beagle dogs. J Periodontol 57, 727, 1986.
217.
Fleisher N., de Waal H., and Bloom A. Regeneration of lost attachment apparatus in the dog using Vicryl absorbable mesh (Polyglactin 910). Int J Periodontics Restorative Dent 8, 44, 1988.
218.
Haney J.M., Nilveus R.E., McMillan P.J., and Wikesjo U.M. Periodontal repair in dogs: expanded polytetrafluoroethylene barrier membranes support wound stabilization and enhance bone regeneration. J Periodontol 64, 883, 1993.
219.
Magnusson I., Stenberg W.V., Batich C., and Egelberg J. Connective tissue repair in circumferential periodontal defects in dogs following use of a biodegradable membrane. J Clin Periodontol 17, 243, 1990.
220.
Tal H., and Pitaru S. Formation of new periodontal attachment apparatus after experimental root isolation with collagen membranes in the dog. Int J Periodont Restorative Dent 12, 231, 1992.
221.
Magnusson I., Batich C., and Collins B.R. New attachment formation following controlled tissue regeneration using biodegradable membranes. J Periodontol 59, 1, 1988.
222.
Pitaru S., Tal H., Soldinger M., Grosskopf A., and Noff M. Partial regeneration of periodontal tissues using collagen barriers—initial observations in the canine. J Periodontol 59, 380, 1988.
223.
Caffesse R.G., Nasjleti C.E., Morrison E.C., and Sanchez R. Guided tissue regeneration: comparison of bioabsorbable and non-bioabsorbable membranes. Histologic and histometric study in dogs. J Periodontol 65, 583, 1994.
224.
Caffesse R.G., Dominguez L.E., Nasjleti C.E., Castelli W.A., Morrison E.C., and Smith B.A. Furcation defects in dogs treated by guided tissue regeneration (GTR). J Periodontol 61, 45, 1990.
225.
Crigger M., Bogle G.C., Garrett S., and Gantes B.G. Repair following treatment of circumferential periodontal defects in dogs with collagen and expanded polytetrafluoroethylene barrier membranes. J Periodontol 67, 403, 1996.
226.
Polimeni G., Susin C., and Wikesjo U.M.E. Regenerative potential and healing dynamics of the periodontium: a critical-size supra-alveolar periodontal defect study. J Clin Periodontol 36, 258, 2009.
227.
Araujo M.G., Berglundh T., Albrekstsson T., and Lindhe J. Bone formation in furcation defects. An experimental study in the dog. J Clin Periodontol 26, 643, 1999.
228.
Pontoriero R., Nyman S., Ericsson I., and Lindhe J. Guided tissue regeneration in surgically-produced furcation defects. An experimental study in the beagle dog. J Clin Periodontol 19, 159, 1992.
229.
Warrer K., and Karring T. Guided tissue regeneration combined with osseous grafting in suprabony periodontal lesions. An experimental study in the dog. J Clin Periodontol 19, 373, 1992.
230.
Stavropoulos A., and Wikesjo U.M. Influence of defect dimensions on periodontal wound healing/regeneration in intrabony defects following implantation of a bovine bone biomaterial and provisions for guided tissue regeneration: an experimental study in the dog. J Clin Periodontol 37, 534, 2010.
231.
Stavropoulos F., Dahlin C., Ruskin J.D., and Johansson C. A comparative study of barrier membranes as graft protectors in the treatment of localized bone defects—an experimental study in a canine model. Clin Oral Implants Res 15, 435, 2004.
232.
Leder A.J., Simon B.I., Deasy M., Fenesy K.E., and Dunn S. Histological, clinical, and digital subtraction radiographic evaluation of repair of periodontal defects resulting from mechanical perforation of the chamber floor using ePTFE membranes. Periodontal Clin Investig 19, 9, 1997.
233.
Robert P.M., and Frank R.M. Periodontal guided tissue regeneration with a new resorbable polylactic acid membrane. J Periodontol 65, 414, 1994.
234.
Bogle G., Garrett S., Stoller N.H., Swanbom D.D., Fulfs J.C., Rodgers P.W., Whitman S., Dunn R.L., Southard G.L., and Polson A.M. Periodontal regeneration in naturally occurring Class II furcation defects in beagle dogs after guided tissue regeneration with bioabsorbable barriers. J Periodontol 68, 536, 1997.
235.
Crigger M., Bogle G., Nilveus R., Egelberg J., and Selvig K.A. The effect of topical citric acid application on the healing of experimental furcation defects in dogs. J Periodontal Res 13, 538, 1978.
236.
Nilveus R., and Egelberg J. The effect of topical citric acid application on the healing of experimental furcation defects in dogs. III. The relative importance of coagulum support, flap design and systemic antibiotics. J Periodontal Res 15, 551, 1980.
237.
Nilveus R., Bogle G., Crigger M., Egelberg J., and Selvig K.A. The effect of topical citric acid application on the healing of experimental furcation defects in dogs. II. Healing after repeated surgery. J Periodontal Res 15, 544, 1980.
238.
Nalbandian J., and Cote N. Direct histological comparison of periodontal wound-healing in the beagle dog with and without citric-acid conditioning. J Periodontal Res 17, 552, 1982.
239.
Bostanci H.S., Arpak M.N., and Gunhan O. New attachment formation following periodontal surgery in a dog. J Nihon Univ Sch Dent 32, 159, 1990.
240.
Bogle G., Claffey N., and Egelberg J. Healing of horizontal circumferential periodontal defects following regenerative surgery in beagle dogs. J Clin Periodontol 12, 837, 1985.
241.
Pettersson E.C., and Aukhil I. Citric acid conditioning of roots affects guided tissue regeneration in experimental periodontal wounds. J Periodontal Res 21, 543, 1986.
242.
Kinoshita A., Oda S., Takahashi K., Yokota S., and Ishikawa I. Periodontal regeneration by application of recombinant human bone morphogenetic protein-2 to horizontal circumferential defects created by experimental periodontitis in beagle dogs. J Periodontol 68, 103, 1997.
243.
Giannobile W.V., Ryan S., Shih M.S., Su D.L., Kaplan P.L., and Chan T.C. Recombinant human osteogenic protein-1 (OP-1) stimulates periodontal wound healing in class III furcation defects. J Periodontol 69, 129, 1998.
244.
Lynch S.E., de Castilla G.R., Williams R.C., Kiritsy C.P., Howell T.H., Reddy M.S., and Antoniades H.N. The effects of short-term application of a combination of platelet-derived and insulin-like growth factors on periodontal wound healing. J Periodontol 62, 458, 1991.
245.
Wang H.L., Pappert T.D., Castelli W.A., Chiego D.J. Jr., Shyr Y., and Smith B.A. The effect of platelet-derived growth factor on the cellular response of the periodontium: an autoradiographic study on dogs. J Periodontol 65, 429, 1994.
246.
Selvig K.A., Wikesjo U.M., Bogle G.C., and Finkelman R.D. Impaired early bone formation in periodontal fenestration defects in dogs following application of insulin-like growth factor (II). Basic fibroblast growth factor and transforming growth factor beta 1. J Clin Periodontol 21, 380, 1994.
247.
Cho M.I., Lin W.L., and Genco R.J. Platelet-derived growth factor-modulated guided tissue regenerative therapy. J Periodontol 66, 522, 1995.
248.
Bianucci H.C., Smith M.M., Saunders G.K., Reddy M.S., Cox C.F., Till L.G., and Feldman B.F. Periodontal healing of canine experimental grade-III furcation defects treated with autologous fibrinogen and absorbable barrier membrane. Am J Vet Res 59, 1329, 1998.
249.
Roriz V.M., Souza S.L.S., Taba M., Palioto D.B., and Grisi M.F.M. Treatment of class III furcation defects with expanded polytetrafluoroethylene membrane associated or not with anorganic bone matrix/synthetic cell-binding peptide: a histologic and histomorphometric study in dogs. J Periodontol 77, 490, 2006.
250.
Kurtis B., Balos K., and Oygur T. Effect of a collagen membrane enriched with fibronectin on guided tissue regeneration in dogs. Periodontal Clin Investig 24, 11, 2002.
251.
Nagayasu-Tanaka T., Anzai J., Takaki S., Shiraishi N., Terashima A., Asano T., Nozaki T., Kitamura M., and Murakami S. Action mechanism of fibroblast growth factor-2 (FGF-2) in the promotion of periodontal regeneration in beagle dogs. PLoS One 10, e0131870, 2015.
252.
Haze A., Taylor A.L., Haegewald S., Leiser Y., Shay B., Rosenfeld E., Gruenbaum-Cohen Y., Dafni L., Zimmermann B., Heikinheimo K., Gibson C.W., Fisher L.W., Young M.F., Blumenfeld A., Bernimoulin J.P., and Deutsch D. Regeneration of bone and periodontal ligament induced by recombinant amelogenin after periodontitis. J Cell Mol Med 13, 1110, 2009.
253.
Watanabe K., Kikuchi M., Okumura M., Kadosawa T., and Fujinaga T. Efficacy of enamel matrix protein applied to spontaneous periodontal disease in two dogs. J Vet Med Sci 65, 1007, 2003.
254.
Sallum E.A., Casati M.Z., Caffesse R.G., Funis L.P., Nociti F.H., and Sallum A.W. Coronally positioned flap with or without enamel matrix protein derivative for the treatment of gingival recessions. Am J Dent 16, 287, 2003.
255.
Sakallioglu U., Acikgoz G., Ayas B., Kirtiloglu T., and Sakallioglu E. Healing of periodontal defects treated with enamel matrix proteins and root surface conditioning-an experimental study in dogs. Biomaterials 25, 1831, 2004.
256.
Pimentel S.P., Sallum A.W., Saldanha J.B., Casati M.Z., Nociti F.H. Jr., and Sallum E.A. Enamel matrix derivative versus guided tissue regeneration in the presence of nicotine: a histomorphometric study in dogs. J Clin Periodontol 33, 900, 2006.
257.
Kanazashi M., Gomi K., Nagano T., Tanabe T., Arai T., and Fukae M. The 17-kDa sheath protein in enamel proteins induces cementum regeneration in experimental cavities created in a buccal dehiscence model of dogs. J Periodontal Res 41, 193, 2006.
258.
Fujita T., Yamamoto S., Ota M., Shibukawa Y., and Yamada S. Coverage of gingival recession defects using guided tissue regeneration with and without adjunctive enamel matrix derivative in a dog model. Int J Periodont Rest 31, 247, 2011.
259.
Cunha-Cruz J., Saver B., Maupome G., and Hujoel P.P. Statin use and tooth loss in chronic periodontitis patients. J Periodontol 77, 1061, 2006.
260.
Tilakaratne A., and Soory M. Anti-inflammatory actions of adjunctive tetracyclines and other agents in periodontitis and associated comorbidities. Open Dent J 8, 109, 2014.
261.
Lee B.S., Lee C.C., Wang Y.P., Chen H.J., Lai C.H., Hsieh W.L., and Chen Y.W. Controlled-release of tetracycline and lovastatin by poly(D,L-lactide-co-glycolide acid)-chitosan nanoparticles enhances periodontal regeneration in dogs. Int J Nanomed 11, 285, 2016.
262.
Kawaguchi H., Hirachi A., Hasegawa N., Iwata T., Hamaguchi H., Shiba H., Takata T., Kato Y., and Kurihara H. Enhancement of periodontal tissue regeneration by transplantation of bone marrow mesenchymal stem cells. J Periodontol 75, 1281, 2004.
263.
Akizuki T., Oda S., Komaki M., Tsuchioka H., Kawakatsu N., Kikuchi A., Yamato M., Okano T., and Ishikawa I. Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. J Periodontal Res 40, 245, 2005.
264.
Hasegawa N., Kawaguchi H., Hirachi A., Takeda K., Mizuno N., Nishimura M., Koike C., Tsuji K., Iba H., Kato Y., and Kurihara H. Behavior of transplanted bone marrow-derived mesenchymal stem cells in periodontal defects. J Periodontol 77, 1003, 2006.
265.
Iwata T., Yamato M., Tsuchioka H., Takagi R., Mukobata S., Washio K., Okano T., and Ishikawa I. Periodontal regeneration with multi-layered periodontal ligament-derived cell sheets in a canine model. Biomaterials 30, 2716, 2009.
266.
Li H., Yan F., Lei L., Li Y., and Xiao Y. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs 190, 94, 2009.
267.
Jiang J., Wu X., Lin M., Doan N., Xiao Y., and Yan F. Application of autologous periosteal cells for the regeneration of class III furcation defects in Beagle dogs. Cytotechnology 62, 235, 2010.
268.
Nunez J., Sanz-Blasco S., Vignoletti F., Munoz F., Arzate H., Villalobos C., Nunez L., Caffesse R.G., and Sanz M. Periodontal regeneration following implantation of cementum and periodontal ligament-derived cells. J Periodontal Res 47, 33, 2012.
269.
Park J.Y., Jeon S.H., and Choung P.H. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant 20, 271, 2011.
270.
Tsumanuma Y., Iwata T., Washio K., Yoshida T., Yamada A., Takagi R., Ohno T., Lin K., Yamato M., Ishikawa I., Okano T., and Izumi Y. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 32, 5819, 2011.
271.
Suaid F.F., Ribeiro F.V., Rodrigues T.L., Silverio K.G., Carvalho M.D., Nociti F.H. Jr., Casati M.Z., and Sallum E.A. Autologous periodontal ligament cells in the treatment of class II furcation defects: a study in dogs. J Clin Periodontol 38, 491, 2011.
272.
Suaid F.F., Ribeiro F.V., Gomes T.R., Silverio K.G., Carvalho M.D., Nociti F.H. Jr., Casati M.Z., and Sallum E.A. Autologous periodontal ligament cells in the treatment of Class III furcation defects: a study in dogs. J Clin Periodontol 39, 377, 2012.
273.
Simsek S.B., Keles G.C., Baris S., and Cetinkaya B.O. Comparison of mesenchymal stem cells and autogenous cortical bone graft in the treatment of class II furcation defects in dogs. Clin Oral Investig 16, 251, 2012.
274.
Tobita M., Uysal C.A., Guo X., Hyakusoku H., and Mizuno H. Periodontal tissue regeneration by combined implantation of adipose tissue-derived stem cells and platelet-rich plasma in a canine model. Cytotherapy 15, 1517, 2013.
275.
Yu X.B., Ge S.H., Chen S.L., Xu Q.C., Zhang J., Guo H.M., and Yang P.S. Human gingiva-derived mesenchymal stromal cells contribute to periodontal regeneration in beagle dogs. Cells Tissues Organs 198, 428, 2013.
276.
Khorsand A., Eslaminejad M.B., Arabsolghar M., Paknejad M., Ghaedi B., Rokn A.R., Moslemi N., Nazarian H., and Jahangir S. Autologous dental pulp stem cells in regeneration of defect created in canine periodontal tissue. J Oral Implantol 39, 433, 2013.
277.
Paknejad M., Eslaminejad M.B., Ghaedi B., Rokn A.R., Khorsand A., Etemad-Moghadam S., Alaeddini M., Dehghan M.M., Moslemi N., and Nowzari H. Isolation and assessment of mesenchymal stem cells derived from bone marrow: histologic and histomorphometric study in a canine periodontal defect. J Oral Implantol 41, 284, 2015.
278.
Zhou W., and Mei L. Effect of autologous bone marrow stromal cells transduced with osteoprotegerin on periodontal bone regeneration in canine periodontal window defects. Int J Periodontics Restorative Dent 32, e174, 2012.
279.
Zhang Y.F., Miron R.J., Li S., Shi B., Sculean A., and Cheng X.R. Novel MesoPorous BioGlass/silk scaffold containing adPDGF-B and adBMP7 for the repair of periodontal defects in beagle dogs. J Clin Periodontol 42, 262, 2015.
280.
England D.C., Winters L.M., and Carpenter L.E. The development of a breed of miniature swine; a preliminary report. Growth 18, 207, 1954.
281.
Wang S., Liu Y., Fang D., and Shi S. The miniature pig: a useful large animal model for dental and orofacial research. Oral Dis 13, 530, 2007.
282.
Larsen M.O., and Rolin B. Use of the Gottingen minipig as a model of diabetes, with special focus on type 1 diabetes research. Ilar J 45, 303, 2004.
283.
Swindle M.M., Makin A., Herron A.J., Clubb F.J., and Frazier K.S. Swine as models in biomedical research and toxicology testing. Vet Pathol 49, 344, 2012.
284.
Weaver M.E., Jump E.B., and McKean C.F. The eruption pattern of deciduous teeth in miniature swine. Anat Rec 154, 81, 1966.
285.
Weaver M.E., Jump E.B., and McKean C.F. The eruption pattern of permanent teeth in miniture swine. Arch Oral Biol 14, 323, 1969.
286.
Gould T.R., Robertson P.B., and Oakley C. Effect of free gingival grafts on naturally-occurring recession in miniature swine. J Periodontol 63, 593, 1992.
287.
Ibi M., Ishisaki A., Yamamoto M., Wada S., Kozakai T., Nakashima A., Iida J., Takao S., Izumi Y., Yokoyama A., and Tamura M. Establishment of cell lines that exhibit pluripotency from miniature swine periodontal ligaments. Arch Oral Biol 52, 1002, 2007.
288.
Sigusch B.W., Pfitzner A., Albrecht V., and Glockmann E. Efficacy of photodynamic therapy on inflammatory signs and two selected periodontopathogenic species in a beagle dog model. J Periodontol 76, 1100, 2005.
289.
Kalkwarf K.L., and Krejci R.F. Effect of inflammation on periodontal attachment levels in miniature swine with mucogingival defects. J Periodontol 54, 361, 1983.
290.
Kalkwarf K.L., Krejci R.F., and Berry W.C. Jr. Chronic mucogingival defects in miniature swine. J Periodontol 54, 81, 1983.
291.
Craig R.G., Kallur S.P., Inoue M., Rosenberg P.A., and LeGeros R.Z. Effect of enamel matrix proteins on the periodontal connective tissue-material interface after wound healing. J Biomed Mater Res A 69A, 180, 2004.
292.
Powell C.A., Bannister S.R., Mackey S.A., Maller S.C., McDonnell H.T., and Deas D.E. Periodontal wound healing with and without platelet-rich plasma: histologic observations and assessment of flap tensile strength. J Periodontol 80, 985, 2009.
293.
Sonoyama W., Liu Y., Fang D.A.J., Yamaza T., Seo B.M., Zhang C.M., Liu H., Gronthos S., Wang C.Y., Shi S.T., and Wang S.L. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 1, e79, 2006.
294.
Ding G., Liu Y., Wang W., Wei F., Liu D., Fan Z., An Y., Zhang C., and Wang S. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 28, 1829, 2010.
295.
Wei F., Qu C., Song T., Ding G., Fan Z., Liu D., Liu Y., Zhang C., Shi S., and Wang S. Vitamin C treatment promotes mesenchymal stem cell sheet formation and tissue regeneration by elevating telomerase activity. J Cell Physiol 227, 3216, 2012.
296.
Fu X.R., Jin L.Y., Ma P., Fan Z.P., and Wang S.L. Allogeneic stem cells from deciduous teeth in treatment for periodontitis in miniature swine. J Periodontol 85, 845, 2014.
297.
Hu J.C., Cao Y., Xie Y.L., Wang H., Fan Z.P., Wang J.S., Zhang C.M., Wang J.S., Wu C.T., and Wang S.L. Periodontal regeneration in swine after cell injection and cell sheet transplantation of human dental pulp stem cells following good manufacturing practice. Stem Cell Res Ther 7, 130, 2016.
298.
Cao Y., Liu Z.H., Xie Y.L., Hu J.C., Wang H., Fan Z.P., Zhang C.M., Wang J.S., Wu C.T., and Wang S.L. Adenovirus-mediated transfer of hepatocyte growth factor gene to human dental pulp stem cells under good manufacturing practice improves their potential for periodontal regeneration in swine. Stem cell Res Ther 6, 249, 2015.
299.
Newman E., Turner A.S., and Wark J.D. The potential of sheep for the study of osteopenia—current status and comparison with other animal-models. Bone 16, S277, 1995.
300.
Cutress T.W. Histopathology of periodontal disease in sheep. J Periodontol 47, 643, 1976.
301.
Baharuddin N.A., Coates D.E., Cullinan M., Seymour G., and Duncan W. Localization of RANK, RANKL and osteoprotegerin during healing of surgically created periodontal defects in sheep. J Periodontal Res 50, 211, 2015.
302.
Duncan W.J., Persson G.R., Sims T.J., Braham P., Pack A.R.C., and Page R.C. Ovine periodontitis as a potential model for periodontal studies—cross-sectional analysis of clinical, microbiological, and serum immunological parameters. J Clin Periodontol 30, 63, 2003.
303.
Mrozik K.M., Wada N., Marino V., Richter W., Shi S.T., Wheeler D.L., Gronthos S., and Bartold P.M. Regeneration of periodontal tissues using allogeneic periodontal ligament stem cells in an ovine model. Regen Med 8, 711, 2013.
304.
Menicanin D., Mrozik K.M., Wada N., Marino V., Shi S.T., Bartold P.M., and Gronthos S. Periodontal-ligament-derived stem cells exhibit the capacity for long-term survival, self-renewal, and regeneration of multiple tissue types in vivo. Stem Cells Dev 23, 1001, 2014.
305.
Daneshmeyer M.J., Pack A.R.C., and Mcmillan M.D. A new animal-model for guided tissue regeneration research. J Dent Res 74, 753, 1995.
306.
DaneshMeyer M.J., Pack A.R.C., and McMillan M.D. A comparison of 2 polytetrafluoroethylene membranes in guided tissue regeneration in sheep. J Periodontal Res 32, 20, 1997.
307.
Gronthos S., Mrozik K., Shi S., and Bartold P.M. Ovine periodontal ligament stem cells: isolation, characterization, and differentiation potential. Calcified Tissue Int 79, 310, 2006.
308.
Mrozik K.M., Zilm P.S., Bagley C.J., Hack S., Hoffmann P., Gronthos S., and Bartold P.M. Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: analysis of differentially expressed proteins. Stem Cells Dev 19, 1485, 2010.
309.
Morinha F., Albuquerque C., Requicha J., Dias I., Leitao J., Gut I., Guedes-Pinto H., Viegas C., and Bastos E. Detection and characterization of interleukin-6 gene variants in Canis familiaris: association studies with periodontal disease. Gene 485, 139, 2011.
310.
Morinha F., Albuquerque C., Requicha J., Dias I., Leitao J., Gut I., Guedes-Pinto H., Viegas C., and Bastos E. Analysis of new lactotransferrin gene variants in a case-control study related to periodontal disease in dog. Mol Biol Rep 39, 4673, 2012.
311.
Albuquerque C., Morinha F., Requicha J., Dias I., Guedes-Pinto H., Viegas C., and Bastos E. A case-control study between interleukin-10 gene variants and periodontal disease in dogs. Gene 539, 75, 2014.

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cover image Tissue Engineering Part C: Methods
Tissue Engineering Part C: Methods
Volume 23Issue Number 12December 2017
Pages: 900 - 925
PubMed: 28795622

History

Published in print: December 2017
Published online: 1 December 2017
Published ahead of print: 25 October 2017
Published ahead of production: 10 August 2017
Accepted: 28 July 2017
Received: 16 March 2017

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Karim M. Fawzy El-Sayed, PhD
Department of Oral Medicine and Periodontology, Faculty of Oral and Dental Medicine, Cairo University, Giza, Egypt.
Clinic for Conservative Dentistry and Periodontology, School of Dental Medicine, Christian Albrechts University, Kiel, Germany.
Christof E. Dörfer, Dr. med. dent
Clinic for Conservative Dentistry and Periodontology, School of Dental Medicine, Christian Albrechts University, Kiel, Germany.

Notes

*
This article is part of a special focus issue on Animal Models in Tissue Engineering. Part II.
Address correspondence to:Karim M. Fawzy El-Sayed, PhDClinic for Conservative Dentistry and PeriodontologySchool of Dental MedicineChristian Albrechts-Universität zu KielArnold-Heller-Straße 3, Haus 26Kiel 24105Germany
E-mail: [email protected]

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No competing financial interests exist.

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