Periodontal Regeneration

Research, Science and Therapy Committee

Available through: The American Academy of Periodontology Scientific, Clinical and Educational Affairs Departmnet 737 North Michigan Avenue, Suite 800 Chicago, Illinois 60611-2690 Phone: (312) 787-5518 Fax: (312) 573-3234

Approved by The Board of Trustees May 1993

PREFACE
Progressive periodontitis leads to tooth loss through destruction of a tooth's attachment apparatus. In teeth in which continued function requires additional periodontal support, optimal treatment involves not only controlling periodontal infection, but also regeneration of the lost periodontium. This paper reviews the results of commonly-used surgical procedures having the objective of regeneration of the lost periodontium. Reports of successful periodontal regeneration have occurred throughout the history of periodontal treatments.1-4 Results following the use of autogenous and allogenic bone grafts, guided tissue regeneration procedures, and alloplastic (synthetic bone substitute) grafts are reviewed. The affect of root surface demineralization and flap management techniques on results following regenerative attempts are also reviewed. Comparisons between clinical studies dealing with periodontal regeneration are difficult because of widely varied methodologies. A synopsis of results and methodology of human clinical studies cited is found in Table I. Results of human histologic studies cited are summarized in Table II. Despite conclusive evidence that some regeneration may occur following regenerative procedures,6-9 complete regeneration is an unrealistic goal. Currently, osseous grafting and guided tissue regeneration are the two techniques with the most histologic documentation of periodontal regeneration.8-12 Other regenerative therapies have also demonstrated merit in terms of significantly improving clinical conditions and demonstrating substantial bone fill.

Copyright ©1993 by The American Acedemy of Periodontology; all rights reserved No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, or otherwise without permission of the Academy.

4 mm. 5 Therefore.13 Histologic evaluation of treated sites in which a reference notch was placed at the alveolar crest demonstrated some supracrestal bone apposition and was strongly suggestive of some periodontal regeneration.5 mm increase in crestal bone height have been reported. and intraosseous defects of various morphologies have been reported.l6 Iliac grafts have been used either fresh or frozen. which predictably filled greater than 50% of the initial defect.25-28 Others have reported the presence of a long junctional epithelium between the regenerated alveolar bone and the root surface in histologic studies of healing following grafting procedures. 1 . New connective tissue attachment is defined as development of a new connective tissue with a root surface that has been deprived of its periodontal ligament. 19. Extraoral Autogenous iliac cancellous bone and marrow is a graft material of high osteogenic potential. Case reports demonstrating successful bone fill after their use in furcations. 23. the difficulties in obtaining the graft material and the possibility of root resorption with fresh grafts have limited their use in clinical practice. Intraoral Intraoral cancellous bone and marrow grafts are usually obtained from the maxillary tuberosity or a healing extraction site. dehiscences. and a new periodontal ligament.2 mm in defects treated with autogenous intraoral grafts. was reported.6 mm in a large number of intraosseous defects and a 2. Root resorption may be a complication following use of fresh grafting techniques. 25-30 Authors have presented histologic evidence of regeneration and new connective tissue attachment following these procedures. 21 Other case reports have shown bone fill following use of cortical bone chips22 and osseous coagulum or bone blend type grafts.DEFINITIONS Regenerative therapy refers to procedures used in the treatment of periodontal disease to achieve replacement/reconstitution of lost periodontal tissues.30 This evidence would suggest that clinically present bone fill is not necessarily a reliable prediction of histologic regeneration of a periodontal attachment apparatus following regenerative procedures. 13-16 Case reports showing a mean bone fill of 3. Bone fill does not address the presence of absence of histologic evidence of new connective tissue attachment. periodontal regeneration is defined as restoration of lost supporting tissues including new alveolar bone. 16-l8 While case reports indicate bone fill and some regeneration may occur following use of grafts of iliac autogenous cancellous bone and marrow. 5 Bone fill is defined as clinical restoration of bone tissue in a previously treated periodontal defect. This occurs by formation of new cementum with inserting collagen fibers. new cementum.3 to 3. BONE GRAFTS Autogenous Bone Grafts.29.24 Histologic evaluations of autogenous intraoral grafts come from case reports. 5 Guided cell repopulation or guided tissue regeneration (GTR) describes procedures designed to manipulate the cells that repopulate the wound healing site to ensure that this repopulation includes cells that lead to regeneration.19-20 A controlled study has indicated a more modest bone fill of 1. Initially published case reports from studies including a large number of intraosseous defects grafted with intraoral bone demonstrated bone fill equal to that obtained with iliac grafts. l9-24 A mean bone fill of 3. Autogenous Bone Grafts.

50 Tissue banks accredited by the American Association of Tissue Banks are required to have procedures in place for testing graft materials for the presence of pathogens. 48 A major concern in the use of allografts is the risk of disease transmission.39 Animal studies 40 indicate that demineralizing bone in 0. have demonstrated periodontal regeneration. freeze-dried bone allografts. Tissues banks have established protocols for obtaining and testing donor materials. other studies suggested that the quantity of BMP in periodontal grafts was too small to induce bone formation 42 and that other proteins may be involved in the osteo-induction process. 36. freeze-dried bone allografts were compared with nongrafted controls and demonstrated no greater bone fill than the non-grafted controls.6 mm. using root notches into existing calculus as the histologic reference point. With proper laboratory techniques and testing. Iliac allografts require cross-matching to decrease the possibility of graft rejection as well as careful screening to prevent the transmission of infectious diseases.0 million if the graft is frozen as a part of processing.34 Controlled clinical trials indicate bone fill ranging from 1. 41 However.6N HC1 followed by freeze drying significantly enhances the osteogenic potential of the allograft. "bone morphogenetic protein" (BMP).44-46 Controlled human histologic studies with this material. i.7 to 2. 35-37 However.4 mm). Allografts from the iliac crest of donors have been used both frozen and sterilized with radiation.67 million or l/8.49.9 mm. Freeze-drying bone allograft material markedly reduces the antigenicity of the allograft. Regeneration achieved with the grafts was significantly more than that in non-grafted controls.3 to 2. 51 Summary There is conclusive evidence that significant bone fill may result after using either autogenous or allogenic bone grafts. 35 Combining freeze-dried bone allografts with tetracycline has shown some promise in treating intraosseous defects resulting from juvenile periodontitis. 4. 42. there are also occasional human studies that indicate similar amounts of bone fill may be achieved following the use of surgical procedures that do not include bone grafts. Potential donors should be screened for histories of neoplastic or infectious disease and materials obtained should be tested for the presence of potential pathogens. However. supposedly by exposing a boneinducing agent called. 33 Field trials have indicated approximately 63% of defects treated with freeze-dried cortical bone allografts show >50% bone fill.43 Human trials using cortical demineralized freeze-dried bone allografts have demonstrated bone fill similar to that achieved with freeze-dried bone allografts ranging from 1. Although favorable clinical results have been reported in case reports31 and more modest results in controlled clinical trials 32. 9 Grafts using decalcified freezedried cancellous bones47 have shown less bone fill (mean 1. 38. 8.e. iliac cancellous bone and marrow. This variation may reflect differences in the amount of bone-inductive proteins in the two tissues. and decalcified freeze-dried bone allografts.52-53 Histologic analysis following grafting procedures indicate that partial periodontal 2 . the difficulties in graft procurement and the need for extensive laboratory facilities and testing limit the clinical usefulness of this material. the risk of disease transfer is calculated to be less than 1/1. in one controlled clinical study.Allogenic Bone Grafts There are several types of bone allografts available from commercial tissue banks.

6l.65-67 Summary Case reports and clinical trials indicate that periodontal intraosseous defects.65 Treatment of maxillary Class II furcation defects and mandibular Class III defects with similar membranes demonstrated clinical improvements as well. 56 Histologic case reports indicate that periodontal regeneration and new connective tissue attachment may also be achieved. 68. significant bone fill has been reported. However. 62 When these procedures are augmented with either autogenous or allogenic grafts. respond favorably with substantial bone fill when treated with guided tissue regeneration techniques including a polytetrafluoroethylene membrane. Several different materials have been used in case reports and clinical studies. 57. the majority of these treated sites have had a remaining residual 3 . but of a more modest and unpredictable degree. with 3-wall defects responding best.64 Results using the polytetrafluoroethylene membrane augmented with decalcified freeze-dried bone allograft 65 or composite grafts of autogenous intraoral grafts and tricalcium phosphate and/or demineralized freezedried bone allografts61 showed substantially more bone fill on reentry of treated furcations.regeneration may occur following use of autogenous and allogenic bone grafts.30 GUIDED CELL REPOPULATION/GUIDED TISSUE REGENERATION It was suggested in 1976 that cells that repopulate the root surface after periodontal surgery will determine the type of attachment that form on the root surface during healing.62 Histologically these changes appear to result from new connective tissue attachmentl1. Early studies used a millipore filter l1 while more recent studies have evaluated an expanded polytetrafluoroethylene membrane. these barriers retard apical migration of epithelium and exclude gingival connective tissue from the healing wound. Some histologic studies indicate the possibility that a long junctional epithelium may exist between newly regenerated alveolar bone and the root surface. the majority of the defects were still considered “open" on reentry. significant clinical improvement and a number of complete clinical defect closures were noted. 69 Similar techniques applied to mandibular Class II furcation defects have produced clinical improvements in terms of decreased probing depths and improved clinical attachment levels. 11. The presence of clinical bone fill does not necessarily indicate periodontal regeneration.63.63 as little bone fill was noted with reentry procedures. results using this approach to treating intraosseous defects seem maintainable over long periods of time.61.57 When this same type of membrane was used in controlled clinical trials treating mandibular Class II furcation defects. Clinically.60 Results using polytetrafluoroethylene membranes to treat intraosseous defects show substantial bone fill averaging approximately 3. 6l. 54 From this hypothesis have come procedures using barrier membranes to allow selective cellular repopulation of the root surface during periodontal regenerative attempts.0 mm either with or without augmentation with graft materials. thus favoring healing influenced primarily from the periodontal ligament space and adjacent alveolar bone.55-58 The fact that this membrane requires a second surgical procedure to remove led to studies reports using biodegradable membranes 37.0 to 5.55-58 Defect selection seems particularly important. In theory.29. especially those characterized by 3 bony walls.59 and autogenous connective tissue grafts as membranes. However. 57.

Twenty-two of 46 furcation defects assessed for bone closure after reentry were judged closed. human clinical trials using flap management techniques designed to enhance clot protection and wound stability have been reported. 74-76 The coronally-positioned flap procedure has been used to treat mandibular Class II furcation detects. It is interesting to note that before reentry the large majority of these "closed" defects demonstrated residual furcal involvement clinically. the flap (wound) margin is generally positioned so that it directly approximates the critical healing area. improvements in probing depths and probing attachment levels were reported. 70.73 Recently. Clinical trails using various resorbable membranes and connective tissue grafts are very preliminary and conclusions regarding their efficacy are premature. If the fibrin linkage is disrupted. These tears or ruptures would delay healing. a new connective tissue attachment to the root surface develops. Histologic results following treatment of supracrestal periodontal defects with this procedure have demonstrated new connective tissue attachment formation with some periodontal regeneration.77 When coronally-positioned flaps were used to treat mandibular Class III furcations. the horizontal portion of the furcation defect had been closed via bone fill. 65-67 FLAP MANAGEMENT Animal research has demonstrated that periodontal wounds can be expected to go through the same generally acknowledged sequence of healing events as all wounds. possibly allowing apical migration of the junctional epithelium. with the formation of a fibrin clot between the flap margin and the root surface. at the conclusion of the study 28 of 32 treated furcations were still clinically classified as Class III defects. 71 Data from animal models suggest that when this initial "fibrin linkage" is maintained during early healing. These results suggest that coronally positioned flaps minimize the influence of the flap (wound) margin during early healing which may influence furcal healing favorably.77 Reentry results from two studies74. 6l. Sites also showed a mean 2. 7l Recently it was suggested that if the tensile strength of the adhering fibrin clot is exceeded.6 mm horizontal bone fill. by volume. In other words. followed by replacement of this fibrin clot by a connective tissue matrix attached to the root surface. However. This procedure positions the flap margin away from the critical healing area (the furcal site) and secures it in that position during early healing time points.78 Summary The concept of wound protection and stability during early healing time points is an appealing one which could conceptually enhance results of regenerative therapy irrespective of the particular surgical technique. Continued clinical research is needed to define the role of this concept in periodontal regeneration.0 mm vertical bone fill and 2. the resulting tear could lead to a regenerative failure.75 indicated an approximate mean 65%.57. a long junctional epithelium type attachment results. Mobility of the flap (wound margin) directly adjacent to the potential regenerative site may overcome the root surface/fibrin clot interface leading to a rupture.furcation defect. 65 Use of polytetrafluoroethylene membranes in treating maxillary Class II and mandibular Class III defects has produced inconsistent results. 72 In regenerative attempts. bone fill in Class II mandibular furcation defects. 4 .

porous hydroxyapatite (replamineform).85 A 5-year followup of non.79 BONE SUBSTlTUTES/ALLOPLASTS These are presently four basic types of alloplastic materials commercially available: nonporous hydroxyapatite. Summary When used as grafts.91 Some histologic studies have demonstrated limited new bone in close approximation to the implant material 92. 99. 88. usually with citric acid. the grafted sites have shown significant clinical improvement compared to non-grafted controls. and HTR polymer (a calcium layered polymer of polymethylmethacrylate and hydroxyethylmethacrylate). unwanted trauma or movement at the flap margin would have little impact on the root surface/fibrin clot interface. Mandibular Class II furcation defects grafted with porous materials have also shown significantly better clinical improvements than non-grafted controls both with and without adjunctive guided tissue regeneration techniques.84. beta tricalcium phosphate.5 to 0.89 While clinical results appear promising. the root surface/wound healing interface is separated from the flap margin. histologically they act as biologic fillers and induce little or no bone fill and very limited if any periodontal regeneration. In controlled clinical trials using both nonporous and porous materials as grafts.Perhaps successful results following procedures that use guided tissue regeneration may provide additional support for the concept of wound protection. It has been reported that porous and nonporous hydroxyapatite materials and HTR are nonresorbable while tricalcium phosphate is resorbable. if regeneration is the desired outcome of the surgical procedure.porous hydroxylapatite implanted intraosseous sites indicated continued clinical stability.6 to 3. Comparisons between bone allografts and hydroxyapatite suggest that they produce clinically similar results. all the alloplast materials seem to produce significantly improved clinical conditions. ADDITIONAL AREAS OF INTEREST Root Surface Demineralization/Citric Acid Root surface demineralization.80-83 The magnitude of defect closure ranged from 1. 72.87. histologically the grafts tend to be encapsulated by connective tissue with minimal or no bone formation. 95 There is also some histologic evidence that a very limited amount of regeneration may be possible following HTR grafts. 96 However. Thus. 97-98 However. at present it appears that alloplastic materials function as a non-irritating filler.90.88 Defects grafted with HTR have also shown significant clinical improvements when compared to non-grafted controls. 102 5 . This technique has been suggested because of its ability to modify the root surface by "detoxifying the surface”10l and exposing collagen fibrils in the cementum or dentin matrix. guided tissue regeneration or osseous grafting seem the more appropriate choice.l00 is often used as a part of regenerative procedures.93 or alongside or within porous graft particles.86 Case reports also indicate defect closure is possible following grafts of tricalcium phosphate. However.7 mm for non-grafted sites.5 mm for grafted sites and 0.94 A single histologic case report suggested that some regeneration may be possible with porous hydroxyapatite grafts. With placement of a membrane.

little if any periodontal regeneration can be expected with their use. 107 Results from clinical.106 Again. when used in humans.Animal studies demonstrated substantial. CONCLUSION Autogenous and allogenic bone grafts have resulted in substantial bone fill in reports involving a large number of case studies. Clinical studies using these techniques to treat other types of periodontal defects have not been reported. 105 Histologic evaluation in some human clinical. Guided tissue regeneration has value as a regenerative procedure particularly in 3-wall intrabony defects. either withoutl08. these histologic results have not been universal. osseous grafts21 or guided tissue regeneration techniques. results in treating class II furcation defects. trials demonstrated new connective tissue attachment and some regeneration following citric acid demineralizatino. this technique did not provide significant clinical. Matrix proteins/growth factors Periodontal research using matrix derived proteins and/or growth factors to expand the amount of predictable regeneration is in the early stages of development. 58. These procedures have shown favorable. although less predictable.l09 or in combination with. new connective tissue attachment following citric acid demineralization71. However. improvements. particularly those involving mandibular teeth. The first human trials were reported in 1991. Alloplastic materials (synthetic bone substitutes) function primarily as biocompatible space fillers. 110 However. 111 In summary. However. trials indicate no additional improvement in clinical. 6 . Clinical and histologic documentation attesting to bone fill and limited periodontal regeneration is sufficient to recommend inclusion of this technique in clinical practice. There is sufficient clinical and histologic documentation of bone fill and some periodontal regeneration to recommend their inclusion in techniques available to the clinician. Histologic evidence seems to suggest that new connective tissue attachment and limited regeneration may result from root surface demineralization. human trials with root surface demineralization have failed to show significant clinical improvement when compared to non-demineralized controls.l04 though a favorable response was not universal.103. procedures.108 Attempts to combine root surface demineralization and fibronectin to induce a more significant regenerative response have shown promise during in-vitro experimentation. 1l2 This interesting and promising area of research is discussed in another research update paper available from the AAP. Flap management techniques to enhance wound stability during early healing time points have produced substantial bone fill in mandibular Class II furcations and limited clinical improvement in mandibular Class III furcations. conditions when citric acid treatment is used in conjunction with surgical.76. this histologic healing pattern does not result in significant improvement in clinical conditions beyond non-demineralized control sites. Use of these materials will produce clinical results similar to osseous grafts or guided tissue regeneration procedures. 6. Controlled clinical trials have shown more modest success.

ABBREVIATION KEY SYMBOLS: ALG ALI AUCT AUE AUI AUO CA CG CP CPA CM CT DEB DFDBA DMM DR F FN FDBA FGG H HA HTR ID MF P λPAL PhA λPPD NAA NB NC PTFE r ra RP RPC SC SM TP X = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = = Allogenic graft Allogenic graft/iliac crest Autogenous connective tissue graft Autogenous graft Autogenous graft/iliac crest Autogenous graft/oral site Citric Acid Collagen Gel Coronally positional flap Coronally positioned flap secured by crown attached sutures Collagen membrane New connective tissue attachment Flap debridement Demineralized freeze dried bone allograft Dura matter membrane Descriptive results Furcation Fibronectin Freeze dried bone allograft Free gingival graft (See table 2 histologic summary) Hydroxyapatite Polymethylmethacrylate + hydroxyethylmethacrylate + calciurn Intraosseous defect Millipore filter Probing bone Change probing attachment level Porous hydroxyapatite Change probing pocket depth New attachment apparatus New bone New cementum Polytetrafluoroethylene membrane Reentry Radiographic assessment Root planed Root planed/currettage Supracrestal defect Submerged defect site Tricalcium phosphate Composite graft autogenous bone + DFDBA or TP 7 .

Summary of Clinical Studies Continued 8 .Table I.

Table I. Summary of Clinical Studies 9 .

Summary of Clinical Studies 10 .Table I.

Table II Summary of Histologic Studies Continued 11 .

Table II Summary of Histologic Studies Continued 12 .

Table I. Summary of Clinical Studies Continued 13 .

Gary Greenstein. and Walter T. Consultant. Garrett. Steven J. Thomas E. William Becker. and W. Armitage. Robert J. Genco. Lee Young. Everett B. Consultant.. Ammons. Max Crigger. Gary C. Meffert. Chairman. William F. Ray C. Robert E. Kornman.Acknowledgments This position paper was authored by Dr. Rees. Van Dyke. Science and Therapy Committee include Drs. Consultant. Max Listgarten. Consultant.. 14 . Ira Lamster. Terry D. Drs. McFall contributed to this paper through peer review. Garrett. Roland M. Kenneth S. Members of the 1992-1993 Research. Jr. Cohen. Steven J. Jr. Williams. Hancock. Consultant.

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