ISPUB.com / IJVM/5/1/3211
  • Author/Editor Login
  • Registration
  • Facebook
  • Google Plus

ISPUB.com

Internet
Scientific
Publications

  • Home
  • Journals
  • Latest Articles
  • Disclaimers
  • Article Submissions
  • Contact
  • Help
  • The Internet Journal of Veterinary Medicine
  • Volume 5
  • Number 1

Original Article

Animal Models in Periodontal Research: A Mini-Review of the Literature

A Dannan, F Alkattan

Keywords

animal models, periodontal disease, periodontology, tissue regeneration

Citation

A Dannan, F Alkattan. Animal Models in Periodontal Research: A Mini-Review of the Literature. The Internet Journal of Veterinary Medicine. 2007 Volume 5 Number 1.

Abstract

Introduction: Animal models have been extensively used in periodontal research to investigate the pathogenesis of periodontal disease, use of dental implants, periodontal tissue regeneration and other procedures. However, there is in the literature a lack of information regarding the frequency of using animal models in periodontal research.

Aim of the study: To address the most preferred animal models demonstrated in the literature within the field of periodontal research.

Methods: A search of the literature in PubMed was performed between March 1967 and February 2008. The search strategy included the combination of the terms “Animal Models” AND “Periodontology”. Inclusion and exclusion criteria of studies were set. Eight subsections of studies were defined; Periodontal Tissue Regeneration Studies, Peri-implant Tissue Studies, Bone Healing Investigations, Periodontitis Model Descriptions, Laser Application, New Animal Model Description, Implant Studies and Bone Regeneration Investigations.

Results: Of the107 studies addressed, only 82 studies met the inclusion criteria. Dogs were the most animal models used (31.16%), monkeys came at the second level (15.58%), and then rats (10.66%), pigs, ferrets and sheep (1.64%) and finally goats (0.82%).

Conclusion: Dogs showed the most animal model used in periodontal research, especially in the periodontal tissue regeneration studies and as periodontal disease models. Monkeys came at a second level and, at last, came other animals. A gold animal model in periodontology does not exist since every application requires a model that fills specific needs.

 

This work was done in the department of Periodontology - Faculty of Dental Medicine – Witten/Herdecke University.

Introduction

Animal models have been used to evaluate the pathogenesis of periodontal diseases and various periodontal treatment modalities. Human longitudinal studies of periodontal diseases pose many problems such as determining the level of disease activity, individuals at risk, and susceptibility to disease progression.

From the viewpoint of comparative biology, non-human primates are similar to humans, having comparable periodontal tissue structures and healthy and diseased periodontal states, as observed in humans (1). However, most non-human primates used for research purposes are large, expensive, and difficult to handle. Furthermore, the genetic background of many of these animals has not been established, because animals used in research are often wild-captured animals, with heterogeneity in age, body weight, and oral and general health conditions (1). Among the species of non- human primates, squirrel monkeys and marmosets are small in size and relatively easy to handle, but unfortunately do not exhibit an inflammatory profile characteristic of human periodontal disease. Periodontal tissue specimens from these animals, unlike humans, exhibit very limited numbers of lymphocytes and plasma cells (2-4).

Rodents, belonging to the cohort Glires, such as mice, rats, and hamsters, have been used widely for periodontal research because of specific advantages such as small size, low cost, known age and genetic background, controllable microflora, and ease of handling and housing (5). However, anatomical structures of periodontal tissues and histopathological features of periodontal disease of rodents are different from those of humans (5). For example, oral sulcular epithelium is keratinized in rodents, but not in humans (6). Neutrophils appear to be the only infiltrating cells in periodontal lesions of rodents. In contrast, periodontally involved human tissues show a complex infiltrate of lymphocytes, plasma cells, macrophages and Neutrophils (5). Suggested reasons for these histological variances include the possibility of some fundamental differences in host responses, or at least in part, some divergence in the reaction of tissues to specific challenges between rodents versus humans (5, 7). Thus, it is clear that efforts to find new animal models which better represent the periodontal disease state in humans would be advantageous for researchers focusing in this area.

The aim of this mini-review was to find out the most preferred animal models demonstrated in the literature in the field of periodontal research during the last two decades.

Review methods

Studies concerning the use of animal models in periodontal research were identified by reviewing the appropriate Medical Subjects Heading (MESH) keywords in the period between March 1967 and February 2008. Standardized methodological filters were used to identify analytical studies included the following keywords: (Animal Models) AND (Periodontology). We also searched reference lists of identified articles and abstracts.

Inclusion criteria

To be eligible for inclusion in the review, studies had to:

  • be pilot studies, cohort studies, description papers or in vivo investigations

  • be in English language

  • consider one or more animal model to investigate one or more subject in the field of periodontology.

Exclusion criteria

Non-English articles, in vitro studies, reviews, case reports, reports of workshops and studies performed on human patients were all excluded from this review. Studies which were addressed without identified texts were also excluded.

To simply arrange the results extracted, we defined 8 subsections of studies as follows:

1- Periodontal Tissue Regeneration Studies (PTRS): contain studies considering growth factors, bone grafts/materials, guided tissue/bone regeneration, Enamel Matrix Derivative (EMD) application, collagen/synthetic membranes, Bone Morphogenetic Proteins (BMPs) application, periodontal tissues' regenerative factors and osteogenesis by means of biological cells.

2- Peri-implant Tissue Studies (PiTS): contain studies considering peri-implant soft and/or hard tissue alterations, peri-implantitis, peri-implant tissue inflammation and treatment of peri-implantitis.

3- Bone Healing Investigations (BHIs): contain studies considering bone healing of artificial defects.

4- Periodontitis Model Descriptions (PMDs): contain studies considering evaluation of assessments in periodontal defects, experimental/induced periodontitis or gingivitis, inflammatory mediators in gingivitis or periodontitis, any animal model of new treatment methods, comparisons between human and animal in terms of periodontal pathogenesis and oral pathology investigations.

5- Laser Application (LA): contain studies considering all applications related to laser.

6- New Animal Model Description (NAMD): contain studies considering evaluation of animals as suitable models in periodontal research and for pioneer treatment ideas.

7- Implant Studies (IS): contain studies considering evaluation of different types of dental implants.

8- Bone Regeneration Investigations (BRIs): contain studies considering bone inducing materials.

Results

The electronic searching system addressed 107 studies, of which, only 82 studies met the inclusion criteria (8), (9), (10), (11), (12), (13), (14, 15), (16), (17), (18), (19), (20), (21), (22), (23), (24), (25), (26), (27, 28), (29), (30), (31), (32), (33), (34, 35), (36, 37), (38-40), (41, 42), (43, 44), (45), (46), (47), (48), (49), (50), (51), (52), (53), (54), (55), (56), (57), (58), (59), (60-62), (63, 64), (65), (66), (67), (68-70), (71), (72), (73), (74), (75), (76), (77), (78), (79), (80), (81), (82), (83), (84), (85), (86), (87), (88, 89) and 25 studies were excluded (90), (91), (92), (93-95), (96, 97), (98), (99, 100), (101, 102), (103, 104), (105), (106), (107-109), (110), (111, 112), (113, 114) (Tables 1 and 2).

Within the 82 studies mentioned, dogs were used as animal models in 38 studies (8), (10), (11), (12), (14, 15), (17), (18), (20), (22), (24), (25), (26), (28), (29), (30), (31), (34, 35), (9), (13), (23), (32), (16), (19), (21), (33), (36, 37), (38), (40), (41), (42), (43), (44), (45), (27), (39).

At the second level, monkeys were used as animal models in 19 studies (46), (47), (53), (56), (60), (48), (54), (52), (49), (55), (59), (62), (61), (63, 64), (51), (58), (57), (50).

Rats came at the third level and were used in periodontal tissue regeneration studies (68-70), (71), (72), (74), (77), in bone healing investigation studies (67), (65) and to describe periodontitis models (75), (76), (66), (73).

Pigs were only mentioned under Peri-implant Tissue Studies (78), (79).

Rabbits were used as animal models in periodontal tissue regeneration studies (80), (82), (83), in laser application (81). Indeed, rabbits were used to describe a new animal model (84).

Ferrets were used to describe periodontitis model in two studies (88, 89).

Sheep were used to describe a new animal model in periodontology (86), (85).

Finally, only one study considered goats in the field of bone regeneration (87).

Figure 1
Table 1: Studies used animal models in periodontal research and the field of application

Figure 2
Table 2: Excluded studies

Discussion

In designing any medical or dental animal study, it is often advantageous to select an animal that is phynogenetically similar to humans. The wide range of animal species allows appropriate selection of bio-models for different investigations. Each species has unique similarities and dissimilarities to humans.

Choosing a gold animal model which suits all fields of application is a current goal in research though seems to be very difficult or impossible.

It was the aim of the current mini-review to address the most frequent animal model used in periodontal research within its different divisions.

According to the electronic search, it was shown that dogs were most used in periodontal research as biological models (31.16%). In view of their docile temperament and natural susceptibility to periodontal disease, dogs, particularly beagles, are used in dental research for the study of periodontal disease progression, guided tissue regeneration, tissue wound healing, and dental implants. The etiologic factors of periodontal disease seem to be identical in humans and dogs (115). Dogs may therefore be of value as a model for experimental gingivitis. In our review, the most frequent use of dogs in the addressed studies was in the field of periodontal tissue regeneration and as models for induced periodontitis. On the other side, dogs were not preferred in implant studies and bone regeneration investigations.

Monkeys came at a second level after dogs (15.58%) and were most considered in periodontal regeneration studies and to investigate periodontitis and/or gingivitis models.

Monkeys have been used widely as an animal model for studying periodontal surgical procedures. Periodontal lesions in these animals are also suitable for evaluating periodontal regenerative procedures (1), especially since histometric analysis needed to quantify the amount of new cementum, periodontal ligament and alveolar bone formed as the result of regenerative periodontal surgery (116), can only be done with animals, usually monkeys or dogs.

Due to the possibility of obtaining block biopsies, the rhesus monkey, cynomolgus monkey, and baboons have been used to study osseointegrated oral implants. Fritz et al. (52) suggested that ligature-induced periodontitis around teeth and ligature-induced peri-implantitis follow similar destructive patterns, namely alteration of microbiological flora.

Although various species of non-human primates are adequate for studying different aspects of periodontal diseases, monkeys are expensive to purchase and maintain and are ferocious (100). However, in the fields of bone healing investigations, laser application and bone regeneration investigations, monkeys were not preferred as resulted in our review.

The laboratory rat, although an acceptable model for studying calculus and caries, has limitations as a model for periodontal disease. That is because periodontal disease in rats is different from that of humans.

In our review, rats came at the third level (10.66%) and were used in periodontal tissue regeneration studies, in bone healing investigation studies and to describe periodontitis models. For other applications, rats were not frequently recommended.

Rabbits came at the forth level (4.1%) and were most used in periodontal tissue regeneration studies. One study considered rabbits in the field of laser application (81). Other study (84) introduced the rabbit as a new animal model and showed that this animal model can be efficiently used for the testing of various bone grafting materials.

Pigs, ferret and sheep came at the fifth level as animal models in periodontal research (1.64%). Pigs where used in peri-implant tissue studies (78, 79) and ferrets were used in two studies to evaluate the clinical and histological characteristics of ligature induced periodontitis (88, 89).

Use of the domestic ferret as an animal study model in periodontics was originally described in the 1940s by King et al., who documented that the occurrence of periodontal disease in ferrets was similar to that occurring in humans (117). The ferret is a suitable model for the study of calculus because of its resemblance to human calculus and the fact that formation of calculus is not diet dependent as in the rat and hamster.

Further research is still needed to ascertain the role of ferrets as a model in the pathogenesis of periodontal disease.

Two studies introduced sheep as new animal models; one of them (85) described a model suitable for training for several periodontal surgical methods and showed that the sheep mandible seems to be a feasible training model for the demonstration and exercise of various periodontal surgical techniques for the treatment of periodontitis. The other study (86) evaluated the sheep as a suitable animal model in which to compare periodontal wound healing after furcation defects were treated with different guided tissue regeneration membranes and showed a successful use of the sheep animal model for guided tissue regeneration research.

Within the results obtained in the current study, only one study (0.82%) (87) used goats to evaluate the clinical applicability and biological behavior of a newly developed injectable calcium phosphate (Ca-P) cement as bone filler for gaps around oral implants.

Conclusion

According to the mini-review of literature achieved in the current study, it could be stated that dogs showed the most animal model used in periodontal research, especially in the periodontal tissue regeneration studies and as periodontal disease models. Monkeys came at a second level and then came rats, rabbits, pigs, ferrets, sheep and goats, each of which was used in a specific field in periodontal research.

This study could have certain limitations due to the research methods used. That is why it was referred to as “mini-review”. However, it is still of importance since no similar reviews has yet been made.

A gold animal model in periodontology does not exist since every application requires a model that fills specific needs.

References

1. Schou S, Holmstrup P, Kornman KS. Non-human primates used in studies of periodontal disease pathogenesis: a review of the literature. J Periodontol. 1993 Jun;64(6):497-508.
2. Adams RA, Zander HA, Polson AM. Interproximal and buccal cell populations apical to the sulcus before and during experimental periodontitis in squirrel monkeys. J Periodontol. 1981 Aug;52(8):416-9.
3. Novak MJ, Polson AM. Effects of levamisole on experimental periodontitis. J Periodontol. 1989 Mar;60(3):137-44.
4. Schectman LR, Ammons WF, Simpson DM, Page RC. 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. 1972;7(3):195-212.
5. Jordan HV. Rodent model systems in periodontal disease research. J Dent Res. 1971 Mar-Apr;50(2):236-42.
6. Takata T, Nikai H, Ijuhin N, Okamoto H. Ultrastructure of regenerated junctional epithelium after surgery of the rat molar gingiva. J Periodontol. 1986 Dec;57(12):776-83.
7. Takata T, Nikai H, Ijuhin N, Ito H. Penetration and uptake of colloidal gold-labeled concanavalin A in the junctional epithelium of the rat. J Periodontol. 1988 Dec;59(12):823-9.
8. Park JB, Lee JY, Park YJ, Rhee SH, Lee SC, Kim TI, et al. Enhanced bone regeneration in beagle dogs with bovine bone mineral coated with a synthetic oligopeptide. J Periodontol. 2007 Nov;78(11):2150-5.
9. Kozlovsky A, Tal H, Laufer BZ, Leshem R, Rohrer MD, Weinreb M, et al. Impact of implant overloading on the peri-implant bone in inflamed and non-inflamed peri-implant mucosa. Clin Oral Implants Res. 2007 Oct;18(5):601-10.
10. Pimentel SP, Sallum AW, Saldanha JB, Casati MZ, Nociti FH, Jr., Sallum EA. Enamel matrix derivative versus guided tissue regeneration in the presence of nicotine: a histomorphometric study in dogs. J Clin Periodontol. 2006 Dec;33(12):900-7.
11. de Vicente JC, Recio O, Martin-Villa L, Junquera LM, Lopez-Arranz JS. Histomorphometric evaluation of guided bone regeneration around implants with SLA surface: an experimental study in beagle dogs. Int J Oral Maxillofac Surg. 2006 Nov;35(11):1047-53.
12. Simion M, Rocchietta I, Kim D, Nevins M, Fiorellini J. Vertical ridge augmentation by means of deproteinized bovine bone block and recombinant human platelet-derived growth factor-BB: a histologic study in a dog model. Int J Periodontics Restorative Dent. 2006 Oct;26(5):415-23.
13. Schwarz F, Jepsen S, Herten M, Sager M, Rothamel D, Becker J. Influence of different treatment approaches on non-submerged and submerged healing of ligature induced peri-implantitis lesions: an experimental study in dogs. J Clin Periodontol. 2006 Aug;33(8):584-95.
14. Jones AA, Buser D, Schenk R, Wozney J, Cochran DL. The effect of rhBMP-2 around endosseous implants with and without membranes in the canine model. J Periodontol. 2006 Jul;77(7):1184-93.
15. Kanazashi M, Gomi K, Nagano T, Tanabe T, Arai T, 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. 2006 Jun;41(3):193-9.
16. Stubinger S, Henke J, Donath K, Deppe H. Bone regeneration after peri-implant care with the CO2 laser: a fluorescence microscopy study. Int J Oral Maxillofac Implants. 2005 Mar-Apr;20(2):203-10.
17. Britain SK, Arx T, Schenk RK, Buser D, Nummikoski P, Cochran DL. The use of guided tissue regeneration principles in endodontic surgery for induced chronic periodontic-endodontic lesions: a clinical, radiographic, and histologic evaluation. J Periodontol. 2005 Mar;76(3):450-60.
18. Stavropoulos F, Dahlin C, Ruskin JD, 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. 2004 Aug;15(4):435-42.
19. Koo KT, Polimeni G, Albandar JM, Wikesjo UM. Periodontal repair in dogs: examiner reproducibility in the supraalveolar periodontal defect model. J Clin Periodontol. 2004 Jun;31(6):439-42.
20. Artzi Z, Givol N, Rohrer MD, Nemcovsky CE, Prasad HS, Tal H. Qualitative and quantitative expression of bovine bone mineral in experimental bone defects. Part 1: Description of a dog model and histological observations. J Periodontol. 2003 Aug;74(8):1143-52.
21. Deppe H, Wagenpfeil S, Donath K. Comparative value of attachment measurements in implant dentistry. Int J Oral Maxillofac Implants. 2004 Mar-Apr;19(2):208-15.
22. Artzi Z, Givol N, Rohrer MD, Nemcovsky CE, Prasad HS, Tal H. Qualitative and quantitative expression of bovine bone mineral in experimental bone defects. Part 2: Morphometric analysis. J Periodontol. 2003 Aug;74(8):1153-60.
23. Conner KA, Sabatini R, Mealey BL, Takacs VJ, Mills MP, Cochran DL. Guided bone regeneration around titanium plasma-sprayed, acid-etched, and hydroxyapatite-coated implants in the canine model. J Periodontol. 2003 May;74(5):658-68.
24. Shibli JA, Martins MC, Nociti FH, Jr., Garcia VG, Marcantonio E, Jr. Treatment of ligature-induced peri-implantitis by lethal photosensitization and guided bone regeneration: a preliminary histologic study in dogs. J Periodontol. 2003 Mar;74(3):338-45.
25. Tehemar S, Hanes P, Sharawy M. Enhancement of osseointegration of implants placed into extraction sockets of healthy and periodontally diseased teeth by using graft material, an ePTFE membrane, or a combination. Clin Implant Dent Relat Res. 2003;5(3):193-211.
26. Shigeno K, Nakamura T, Inoue M, Ueda H, Kobayashi E, Nakahara T, et al. Regenerative repair of the mandible using a collagen sponge containing TGF-beta1. Int J Artif Organs. 2002 Nov;25(11):1095-102.
27. Deppe H, Horch HH, Henke J, Donath K. Per-implant care of ailing implants with the carbon dioxide laser. Int J Oral Maxillofac Implants. 2001 Sep-Oct;16(5):659-67.
28. Nociti FH, Jr., Machado MA, Stefani CM, Sallum EA. Absorbable versus nonabsorbable membranes and bone grafts in the treatment of ligature-induced peri-implantitis defects in dogs: a histometric investigation. Int J Oral Maxillofac Implants. 2001 Sep-Oct;16(5):646-52.
29. Isaka J, Ohazama A, Kobayashi M, Nagashima C, Takiguchi T, Kawasaki H, et al. Participation of periodontal ligament cells with regeneration of alveolar bone. J Periodontol. 2001 Mar;72(3):314-23.
30. Hosokawa R, Kikuzaki K, Kimoto T, Matsuura T, Chiba D, Wadamoto M, et al. Controlled local application of basic fibroblast growth factor (FGF-2) accelerates the healing of GBR. An experimental study in beagle dogs. Clin Oral Implants Res. 2000 Aug;11(4):345-53.
31. Ruskin JD, Hardwick R, Buser D, Dahlin C, Schenk RK. Alveolar ridge repair in a canine model using rhTGF-beta 1 with barrier membranes. Clin Oral Implants Res. 2000 Apr;11(2):107-15.
32. Machado MA, Stefani CM, Sallum EA, Sallum AW, Tramontina VA, Nociti Junior FH. Treatment of ligature-induced peri-implantitis defects by regenerative procedures: a clinical study in dogs. J Oral Sci. 1999 Dec;41(4):181-5.
33. Holland M, Boring JG, Boyle CR, Pickrum HM, Jeffcoat MK. Radiographic bone loss correlations and technetium-99m-MDP bone uptake in ligature-induced periodontal disease in the beagle. Vet Radiol Ultrasound. 1998 Jul-Aug;39(4):366-74.
34. Caplanis N, Sigurdsson TJ, Rohrer MD, Wikesjo UM. Effect of allogeneic, freeze-dried, demineralized bone matrix on guided bone regeneration in supra-alveolar peri-implant defects in dogs. Int J Oral Maxillofac Implants. 1997 Sep-Oct;12(5):634-42.
35. Leder AJ, Simon BI, Deasy M, Fenesy KE, 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. 1997 Fall;19(2):9-15.
36. Paquette DW, Fiorellini JP, Martuscelli G, Oringer RJ, Howell TH, McCullough JR, et al. Enantiospecific inhibition of ligature-induced periodontitis in beagles with topical (S)-ketoprofen. J Clin Periodontol. 1997 Aug;24(8):521-8.
37. Skaleric U, Kramar B, Petelin M, Pavlica Z, Wahl SM. Changes in TGF-beta 1 levels in gingiva, crevicular fluid and serum associated with periodontal inflammation in humans and dogs. Eur J Oral Sci. 1997 Apr;105(2):136-42.
38. Haney JM, Zimmerman GJ, Wikesjo UM. Periodontal repair in dogs: evaluation of the natural disease model. J Clin Periodontol. 1995 Mar;22(3):208-13.
39. Jensen OT, Greer RO, Jr., Johnson L, Kassebaum D. Vertical guided bone-graft augmentation in a new canine mandibular model. Int J Oral Maxillofac Implants. 1995 May-Jun;10(3):335-44.
40. Wikesjo UM, Kean CJ, Zimmerman GJ. Periodontal repair in dogs: supraalveolar defect models for evaluation of safety and efficacy of periodontal reconstructive therapy. J Periodontol. 1994 Dec;65(12):1151-7.
41. Kryshtalskyj E, Sodek J, Ferrier JM. Correlation of collagenolytic enzymes and inhibitors in gingival crevicular fluid with clinical and microscopic changes in experimental periodontitis in the dog. Arch Oral Biol. 1986;31(1):21-31.
42. van Dijk LJ, Jansen J, Pilot T, van der Weele LT. Artificial periodontal defects in beagle dogs. A clinical evaluation during 24 months. J Periodontol. 1982 Jul;53(7):449-52.
43. Matsson L, Attstrom R. Development of experimental gingivitis in the juvenile and adult beagle dog. J Clin Periodontol. 1979 Jun;6(3):186-93.
44. Rylander H, Attstrom R, Lindhe J. Influence of experimental neutropenia in dogs with chronic gingivitis. J Periodontal Res. 1975 Dec;10(6):315-23.
45. Hull PS, Davies RM, Lennon MA. The use of the beagle dog as a model system for investigations of anti-plaque agents. J Periodontal Res. 1972(10):37-8.
46. Teare JA, Ramoshebi LN, Ripamonti U. Periodontal tissue regeneration by recombinant human transforming growth factor-beta 3 in Papio ursinus. J Periodontal Res. 2008 Feb;43(1):1-8.
47. Blumenthal NM, Alves ME, Al-Huwais S, Hofbauer AM, Koperski RD. Defect-determined regenerative options for treating periodontal intrabony defects in baboons. J Periodontol. 2003 Jan;74(1):10-24.
48. Sculean A, Junker R, Donos N, Berakdar M, Brecx M, Dunker N. Immunohistochemical evaluation of matrix molecules associated with wound healing following regenerative periodontal treatment in monkeys. Clin Oral Investig. 2002 Sep;6(3):175-82.
49. Oates TW, Graves DT, Cochran DL. Clinical, radiographic and biochemical assessment of IL-1/TNF-alpha antagonist inhibition of bone loss in experimental periodontitis. J Clin Periodontol. 2002 Feb;29(2):137-43.
50. Fritz ME, Jeffcoat MK, Reddy M, Koth D, Braswell LD, Malmquist J, et al. Implants in regenerated bone in a primate model. J Periodontol. 2001 Jun;72(6):703-8.
51. Ebersole JL, Cappelli D, Mathys EC, Steffen MJ, Singer RE, Montgomery M, et al. Periodontitis in humans and non-human primates: oral-systemic linkage inducing acute phase proteins. Ann Periodontol. 2002 Dec;7(1):102-11.
52. Fritz ME, Braswell LD, Koth D, Jeffcoat M, Reddy M, Cotsonis G. Experimental peri-implantitis in consecutively placed, loaded root-form and plate-form implants in adult Macaca mulatta monkeys. J Periodontol. 1997 Nov;68(11):1131-5.
53. Rajnay ZW, Butler JR, Vernino AR, Parker DE. Volumetric changes following barrier regeneration procedures for the surgical management of grade II molar furcation defects in baboons: I. Overall defect fill. Int J Periodontics Restorative Dent. 1997 Aug;17(4):378-91.
54. Hanisch O, Cortella CA, Boskovic MM, James RA, Slots J, Wikesjo UM. Experimental peri-implant tissue breakdown around hydroxyapatite-coated implants. J Periodontol. 1997 Jan;68(1):59-66.
55. Miller DR, Aufdemorte TB, Fox WC, Waldrop TC, Mealey BL, Brunsvold MA. Periodontitis in the baboon: a potential model for human disease. J Periodontal Res. 1995 Nov;30(6):404-9.
56. Ling LJ, Lai YH, Hwang H, Chen H. Response of regenerative tissues to plaque: a histological study in monkeys. J Periodontol. 1994 Aug;65(8):781-7.
57. Fritz ME, Lemons JE, Jeffcoat M, Braswell LD, Reddy M. Evaluation of consecutively placed unloaded root-form and plate-form implants in adult Macaca mulatta monkeys. J Periodontol. 1994 Aug;65(8):788-95.
58. Persson GR, Engel LD, Whitney CW, Weinberg A, Moncla BJ, Darveau RP, et al. Macaca fascicularis as a model in which to assess the safety and efficacy of a vaccine for periodontitis. Oral Microbiol Immunol. 1994 Apr;9(2):104-11.
59. Persson GR, Engel LD, Moncla BJ, Page RC. Macaca nemestrina: a non-human primate model for studies of periodontal disease. J Periodontal Res. 1993 Jul;28(4):294-300.
60. Berg JO, Blomlof L, Lindskog S. Cellular reactions in pulpal and periodontal tissues after periodontal wound debridement. J Clin Periodontol. 1990 Mar;17(3):165-73.
61. Birek P, McCulloch CA, Overall CM. Measurements of probing velocity with an automated periodontal probe and the relationship with experimental periodontitis in the Cynomolgus monkey (Macaca fascicularis). Arch Oral Biol. 1989;34(10):793-801.
62. McMahon KT, Wasfy MO, Yonushonis WP, Minah GE, Falkler WA, Jr. Comparative microbiological and immunological studies of subgingival dental plaque from man and baboons. J Dent Res. 1990 Jan;69(1):55-9.
63. Krygier G, Genco RJ, Mashimo PA, Hausmann E. Experimental gingivitis in Macaca speciosa monkeys: clinical, bacteriologic and histologic similarities to human gingivitis. J Periodontol. 1973 Aug;44(8):454-63.
64. Listgarten MA, Ellegaard B. Experimental gingivitis in the monkey. Relationship of leukocyte counts in junctional epithelium, sulcus depth, and connective tissue inflammation scores. J Periodontal Res. 1973;8(4):199-214.
65. Develioglu H, Saraydin SU, Dupoirieux L, Sahin ZD. Histological findings of long-term healing of the experimental defects by application of a synthetic biphasic ceramic in rats. J Biomed Mater Res A. 2007 Feb;80(2):505-8.
66. Xu Y, Wei W. A comparative study of systemic subantimicrobial and topical treatment of minocycline in experimental periodontitis of rats. Arch Oral Biol. 2006 Sep;51(9):794-803.
67. Gurgel BC, Ribeiro FV, Silva MA, Nociti FH, Jr., Sallum AW, Sallum EA, et al. Selective COX-2 inhibitor reduces bone healing in bone defects. Braz Oral Res. 2005 Oct-Dec;19(4):312-6.
68. Donos N, Kostopoulos L, Karring T. Alveolar ridge augmentation using a resorbable copolymer membrane and autogenous bone grafts. An experimental study in the rat. Clin Oral Implants Res. 2002 Apr;13(2):203-13.
69. Donos N, Kostopoulos L, Karring T. Augmentation of the rat jaw with autogeneic cortico-cancellous bone grafts and guided tissue regeneration. Clin Oral Implants Res. 2002 Apr;13(2):192-202.
70. Donos N, Kostopoulos L, Karring T. Alveolar ridge augmentation by combining autogenous mandibular bone grafts and non-resorbable membranes. Clin Oral Implants Res. 2002 Apr;13(2):185-91.
71. Salata LA, Hatton PV, Devlin AJ, Craig GT, Brook IM. In vitro and in vivo evaluation of e-PTFE and alkali-cellulose membranes for guided bone regeneration. Clin Oral Implants Res. 2001 Feb;12(1):62-8.
72. Ohnishi H, Fujii N, Futami T, Taguchi N, Kusakari H, Maeda T. A histochemical investigation of the bone formation process by guided bone regeneration in rat jaws. Effect of PTFE membrane application periods on newly formed bone. J Periodontol. 2000 Mar;71(3):341-52.
73. Mehrara BJ, Saadeh PB, Steinbrech DS, Dudziak M, Grayson BH, Cutting CB, et al. A rat model of gingivoperiosteoplasty. J Craniofac Surg. 2000 Jan;11(1):54-8.
74. Somerman MJ, Ouyang HJ, Berry JE, Saygin NE, Strayhorn CL, D'Errico JA, et al. Evolution of periodontal regeneration: from the roots' point of view. J Periodontal Res. 1999 Oct;34(7):420-4.
75. Hayashi A, Shinohara M, Ohura K. Effect of insulin on naturally occurring gingivitis rats with diabetes. J Osaka Dent Univ. 1999 Apr;33(1):1-7.
76. Morisaki I, Kato K, Loyola-Rodriguez JP, Nagata T, Ishida H. Nifedipine-induced gingival overgrowth in the presence or absence of gingival inflammation in rats. J Periodontal Res. 1993 Nov;28(6 Pt 1):396-403.
77. Shklar G. Experimental oral pathology in the Syrian hamster. Prog Exp Tumor Res. 1972;16:518-38.
78. Singh G, O'Neal RB, Brennan WA, Strong SL, Horner JA, Van Dyke TE. Surgical treatment of induced peri-implantitis in the micro pig: clinical and histological analysis. J Periodontol. 1993 Oct;64(10):984-9.
79. Hickey JS, O'Neal RB, Scheidt MJ, Strong SL, Turgeon D, Van Dyke TE. Microbiologic characterization of ligature-induced peri-implantitis in the microswine model. J Periodontol. 1991 Sep;62(9):548-53.
80. Verschueren DS, Gassner R, Mitchell R, Mooney MP. The effects of guided tissue regeneration (GTR) on modified Le Fort I osteotomy healing in rabbits. Int J Oral Maxillofac Surg. 2005 Sep;34(6):650-5.
81. Nikolopoulos S, Naoumidou I, Nikolopoulou M, Helidonis E, Castanas E. ArF-193 excimer laser and Emdogain in the treatment of experimental periodontitis: an experimental study in rabbits. Photomed Laser Surg. 2004 Aug;22(4):357-62.
82. Caiazza S, Colangelo P, Bedini R, Formisano G, De Angelis G, Barrucci S. Evaluation of guided bone regeneration in rabbit femur using collagen membranes. Implant Dent. 2000;9(3):219-25.
83. Schmitt JM, Buck DC, Joh SP, Lynch SE, Hollinger JO. Comparison of porous bone mineral and biologically active glass in critical-sized defects. J Periodontol. 1997 Nov;68(11):1043-53.
84. el-Bokle D, Smith SJ, Germane N, Sharawy M. New technique for creating permanent experimental alveolar clefts in a rabbit model. Cleft Palate Craniofac J. 1993 Nov;30(6):542-7.
85. Al-Qareer AH, Afsah MR, Muller HP. A sheep cadaver model for demonstration and training periodontal surgical methods. Eur J Dent Educ. 2004 May;8(2):78-83.
86. Danesh-Meyer MJ, Pack AR, McMillan MD. A comparison of 2 polytetrafluoroethylene membranes in guided tissue regeneration in sheep. J Periodontal Res. 1997 Jan;32(1 Pt 1):20-30.
87. Comuzzi L, Ooms E, Jansen JA. Injectable calcium phosphate cement as a filler for bone defects around oral implants: an experimental study in goats. Clin Oral Implants Res. 2002 Jun;13(3):304-11.
88. Fischer RG, Klinge B. Clinical and histological evaluation of ligature-induced periodontal breakdown in domestic ferrets immunosuppressed by Cyclosporin-A. J Clin Periodontol. 1994 Apr;21(4):240-9.
89. Fischer RG, Klinge B. Clinical and histological evaluation of ligature-induced periodontitis in the domestic ferret. J Clin Periodontol. 1994 Apr;21(4):230-9.
90. Motsonelidze NR, Okropiridze TV, Kapanadze RV. [Usage of Cerasorbe in complex treatment of chronic generalized periodontitis (clinical-experimental study)]. Georgian Med News. 2005 Jan(118):17-20.
91. Romanos GE, Henze M, Banihashemi S, Parsanejad HR, Winckler J, Nentwig GH. Removal of epithelium in periodontal pockets following diode (980 nm) laser application in the animal model: an in vitro study. Photomed Laser Surg. 2004 Jun;22(3):177-83.
92. Lanning SK, Waldrop TC, Gunsolley JC, Maynard JG. Surgical crown lengthening: evaluation of the biological width. J Periodontol. 2003 Apr;74(4):468-74.
93. Dahlen G. Microbiology and treatment of dental abscesses and periodontal-endodontic lesions. Periodontol 2000. 2002;28:206-39.
94. Grigor'ian AS, Frolova OA, Ivanova EV. [Morphogenesis of early stages of periodontal inflammations]. Stomatologiia (Mosk). 2002;81(1):19-25.
95. Rupprecht RD, Horning GM, Towle HJ, 3rd. A clinical evaluation of hydroxyapatite cement in the treatment of Class III furcation defects. J Periodontol. 2001 Oct;72(10):1443-50.
96. Baron M, Haas R, Dortbudak O, Watzek G. Experimentally induced peri-implantitis: a review of different treatment methods described in the literature. Int J Oral Maxillofac Implants. 2000 Jul-Aug;15(4):533-44.
97. Maddox E, Zhan M, Mundy GR, Drohan WN, Burgess WH. Optimizing human demineralized bone matrix for clinical application. Tissue Eng. 2000 Aug;6(4):441-8.
98. Otis LL, Colston BW, Jr., Everett MJ, Nathel H. Dental optical coherence tomography: a comparison of two in vitro systems. Dentomaxillofac Radiol. 2000 Mar;29(2):85-9.
99. Gatti A, Monari E, Tanza D, Betti V. [Evaluation of the biocompatibility of grafts for bone defects]. Minerva Stomatol. 1999 Jun;48(6 Suppl 1):47-52.
100. Weinberg MA, Bral M. Laboratory animal models in periodontology. J Clin Periodontol. 1999 Jun;26(6):335-40.
101. Campan P, Planchand PO, Duran D. Pilot study on n-3 polyunsaturated fatty acids in the treatment of human experimental gingivitis. J Clin Periodontol. 1997 Dec;24(12):907-13.
102. Cochran DL. Report of the American Academy of Periodontology's Workshop on the Design and Conduct of Clinical Trials for Endosseous Dental Implants. J Periodontol. 1998 Feb;69(2):280-4.
103. Caton JG. Overview of clinical trials on periodontal regeneration. Ann Periodontol. 1997 Mar;2(1):215-22.
104. Singleton DG, Torres-Cabassa A. Regulatory issues relating to therapies for periodontal regeneration. Ann Periodontol. 1997 Mar;2(1):223-8.
105. Howell TH, Martuscelli G, Oringer J. Polypeptide growth factors for periodontal regeneration. Curr Opin Periodontol. 1996;3:149-56.
106. Marshall MV, Cancro LP, Fischman SL. Hydrogen peroxide: a review of its use in dentistry. J Periodontol. 1995 Sep;66(9):786-96.
107. Steinberg LM, Strom JL, Harbo JN, Mandel ID. The squirrel monkey as a model in gingivitis studies. Quintessence Int. 1986 Feb;17(2):113-8.
108. Stosser L, Kneist S, Grosser W, Kunzel W. [Root caries--a rat model]. Zahn Mund Kieferheilkd Zentralbl. 1989;77(7):655-8.
109. Flores-de-Jacoby L. [Periodontal treatment after the method of guided periodontal tissue regeneration]. Dtsch Zahnarztl Z. 1991 Jun;46(6):390-3.
110. Ritter G, Sponholz H, Blau HJ. [Relationship between acute leukemia in childhood and periodontal diseases]. Stomatol DDR. 1980 Oct;30(10):722-30.
111. Krook L, Whalen JP, Lesser GV, Berens DL. Experimental studies on osteoporosis. Methods Achiev Exp Pathol. 1975;7:72-108.
112. Schneider AR, Zaka AE. Gingival wound healing following experimental electrosurgery: an electron microscopic investigation. J Periodontol. 1974 Sep;45(9):685-94.
113. Glickman I, Smulow JB, Moreau J. Postsurgical periodontal healing in alloxan diabetes. J Periodontol. 1967 Mar-Apr;38(2):93-9.
114. Schneider HG. [Albino rat as an experimental animal in experimental periodontology]. Dtsch Stomatol. 1972 Aug;22(8):599-607.
115. Ericsson I, Lindhe J, Rylander H, Okamoto H. Experimental periodontal breakdown in the dog. Scand J Dent Res. 1975 May;83(3):189-92.
116. Caton J, Mota L, Gandini L, Laskaris B. Non-human primate models for testing the efficacy and safety of periodontal regeneration procedures. J Periodontol. 1994 Dec;65(12):1143-50.
117. King J, Gimson A Experimental investigations of periodontal disease in the ferret and related lesions in man. British Dental Journal 1947;83:126-7.

Author Information

Aous Dannan, M.Sc.
Department of Periodontology, Faculty of Dental Medicine, Witten/Herdecke University

Farah Alkattan, D.D.S.
Department of Oral Surgery, Faculty of Dental Medicine, Witten/Herdecke University

Download PDF

Your free access to ISPUB is funded by the following advertisements:

 

BACK TO TOP
  • Facebook
  • Google Plus

© 2013 Internet Scientific Publications, LLC. All rights reserved.    UBM Medica Network Privacy Policy