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BARRIER MEMBRANE TECHNIQUES IN ENDODONTIC MICROSURGERY PECORA et al

VOLUME 41. NUMBER 3. JULY 1997 1 16

MICROSCOPES IN ENDODONTICS 0011-8532/97 $0.00 + .20

BARRIER MEMBRANETECHNIQUES IN ENDODONTIC

MICROSURGERY

Gabriele Pecora, MD, DDS, Seung-Ho Baek, DDS, PhDSivakami Rethnam, BDS, and Syngcuk Kim, DDS, M Phil, PhD

The ultimate goal of endodontic microsurgery is the predictable regeneration of periapical tissues,including a complete repair of osseous defects. It is important first to distinguish between regeneration andrepair. Regeneration is the replacement of destroyed tissue with new tissue formed by the cells of the sameorigin. This new tissue reacts in a similar manner against pathologic stimuli. Repair is the restoration of thetissue destroyed by disease with new tissue consisting of cells different from the original cells. These cellsreact differently from the original cells against pathologic stimuli.

One of main concerns in treating an endodontically involved tooth that has a through-and-through osseousdefect is that incomplete bone healing may be inevitable .1, 211 Ingrowth of connective tissue into theosseous defect prevents periapical bone regeneration. The ingrowth of connective tissue can result inperiapical scarring, which is often misdiagnosed as pathology and may lead to unnecessary surgical reentry bya practitioner who is not fully aware of the history. When the barrier membranes are placed over bony defectsand closely adapted to the surrounding bone surface, an environment that prevents invasion of competing

nonosteogenic cells from the overlying soft tissues can be created. This environment provides the bony defecttime to heal.Guided tissue regeneration (GTR) is a procedure used to regenerate lost attachment apparatus throughdifferential tissue response. The objective of GTR in endodontic microsurgery is to enhance the quality andquantity of bone regeneration in the periapical region and to accelerate bone growth in circumscribed bonecavities after endodontic surgery.

From the Department of Endodontics, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania (GP,S-HB, SR, SK); and the Department of Conservative Dentistry, Dental College, Seoul National University, Seoul, Korea(SHB)

DENTAL CLINICS OF NORTH AMERICA


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CLINICAL APPLICATION OF GUIDED TISSUEREGENERATION IN ENDODONTIC MICROSURGERY

The first commercially available barrier membrane was an expanded polytetrafluoroethylene (ePTFE)called Gore- Tex (W.L. Gore, Inc., Flagstaff, AZ) periodontal membrane. This membrane is nonresorbableand requires a second surgical procedure for its removal. Today, barrier materials can be classified into two

groups: resorbable and nonresorbable. Resorbable materials include collagen, calcium sulfate, polyglacticacid, polylactic acid, a copolymer of file two materials, 13 and membranes made of laminar bone (Lambone,Pacific Coast Tissue Bank, Los Angeles, CA). Resorbable barriers undergo resorption by enzymatic orcellular mediated mechanisms by the recipient host. Nonresorbable membranes include polytetrafluorethylene(PTFE); Gore-Tex, which is expanded. Table 1 lists the different types of materials used as barriers.

RATIONALE FOR GUIDED TISSUE REGENERATION INENDODONTIC MICROSURGERY

Periapical lesions healing with scar tissue after surgical treatment of periapical granulomas or cysts wasdescribed by Andreason and Rud.1, 111 Histologic changes were studied in 70 biopsy specimens from lessthan 1 year to 14 years after endodontic surgery. Healing following periapical surgery can be categorized intothree main types: reformation of the periodontal membrane, fibrous tissue or scar tissue with varying gradesof inflammation, and moderate to severe periapical inflammation without scar tissue formation.

It was concluded that fibrous scar tissue is probably formed by the rapidly proliferating epithelial andconnective tissue cells outpacing the slower periodontal ligament and bone regeneration from the cavity.

The size of the circumscribed lesion was found to be of great importance in bone healing in numerousanimal experiments', 14,29 because the distance between the soft and hard tissues determines which kind of tissue is formed. If fibrous tissue has been established first, it will probably act as a barrier against furtherbone formation. Kaban and Glowacki 16 created 4-mm diameter through-and through defects in themandibular ramus of rats. These defects failed to heal at 16 and 24 weeks. Hjorting-Hansen and Andreasen14

created 5-mm, 6-mm, and 8nun defects in the mandible of adult mongrel dogs. At 16 weeks, 8-mm defectsexhibited healing with fibrous tissue. Schmitz and Hollinger29 suggested 20-mm defects as the critical sizethat would not heal in a monkey mandible.

Dahlin and colleagues9, 111 were the first to apply the concept of GTR to bone surgery, creating theguided bone regeneration (GBR), or osteopromotion with membrane, and subsequently applied it toendodontic surgery. In 1988, it was concluded that "the placement of membranes to bony lesions led to acomplete bony restitution of the defects." In 1990, Dahlin and colleagues10 evaluated the healing of maxillaryand mandibular bone defects using the membrane technique in the monkey model. Bilateral transosseousdefects were created in

Table 1. TYPES OF BARRIERS

Resorbable Nonresorbable

Polylactic acid (Guidor, Resolute) PTFE (Gore-Tex)Polyglactic acid (Vicryl) Rubber damCollagen (Biomend, Paroguide, CollaTape)Fasciaalcium sulfate (Surgi Plaster)


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edentulous areas of the maxilla and the mandible, following apicoectomy on the lateral incisor.It was observed that when a membrane was used, all the surgical sites healed with an almost complete closurewith newly formed bone. A cementum-like tissue, with inserting collagen fibers, was found on the cuttingsurface. In the control surgical sites, where no membrane was used, the bone defects were filled with fibrousconnective tissue, characterized by collagen fibers parallel to the root surfaces. Cortical bone did not gain itscontinuity both buccally and lingually. None of the teeth showed cementum, on the cutting surface.

A physical barrier may impede the colonization of the bone defect by the fibroblasts from the surroundingconnective tissue such as the inner surface of the flap. Thus, there is no competition for osteogenesis (Figs.1-3).14, 111 The use of barrier membranes in endodontic surgery was advocated by Diggins and co-workers"for the management of root perforations, by Pecora and colleagueS25 for the management of large periapicallesions, and by Rankow and Krasner27 in general to endodontic surgery.

Baek and associates2 evaluated whether improved bone regeneration can be achieved inthrough-and-through osseous defects in ferrets with a nondegradable membrane barrier (Gore-Tex) and twobiodegradable membrane barriers (Vicryl, Ethicon, East Brunswick, Nj; Guidor, Guidor Co, Bensenville, IL).In each group, the defects were covered both buccally and lingually with a Gore-Tex membrane and Vicryl orGuidor membrane (see Fig. 1). The control group, which did not receive any membrane barrier, did not showany substantial bone regeneration. The Gore-Tex and Vicryl group showed good osteoconductive potentialwith almost complete lamellar bone filling. Histologically, bone regeneration in membrane barrier defectsshowed the following patterns of bone growth. In first stage, the woven bone was formed rapidly, and

Figure 1. Immediately following endodontic microsurgery. Proliferation of cells from the soft tissue, PDL, and bone.

primary spongiosa was formed. Second stage was the formation of parallel-fibered and lamellar bone. The

third stage was characterized by cancellous and cortical bone remodeling. The results of this study suggestedthat membrane barrier technique generally improved the bone regeneration in through-and-through periapicaldefects.


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Figure 2. Cells from the soft tissue outpacing slower-growing PDL and osteogenic cells.

Figure 3. Placement of a barrier prevents soft-tissue invasion of the bony crypt, allowing bone to "fill in."

A study by Cortellini and associates7 that compared the clinical efficacy and predictability of somebioresorbable and nonresorbable membranes in periodontology concluded that both membrane types resultedin clinically and statistically significant improvements in the clinical attachment levels and probing depths. Theuse of either of these barriers was equally effective and significantly better than conventional access flaps. Ithas been demonstrated that the effectiveness of the biologic principle of the selective repopulation of thehealing wound is independent of the type of barrier material .5

Table 2 lists indications for GTR application in endodontic microsurgery. Some points to remember whileusing barrier membranes are:

1. The membranes should extend at least 2 to 3 mm beyond the margins of the bone cavity.

2. A secluded space must be created underneath the membrane to allow the growth of newtissue.


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3. The membrane should be totally submerged because exposed membrane increases the risk of infection.4. The membrane must be stable and immovable.5. The membrane must act as a selective barrier for at least 6 to 8 weeks.6. Mobile teeth must be splinted.7. A strict oral hygiene regimen must be followed.

Pecora and colleagues25

.reported the clinical application of GTR with I-year postoperative results.Twenty patients with large endodontic lesions that failed to respond to conventional endodontic therapy wereselected. The lesions had a radiographic diameter of at least 10 mm. They were surgically removed followedby apicoectomy and retrograde filling with either SuperEBA or desiccated ZOE. In 10 test sites, largeGore-Tex was used. Radiographic analysis of the lesion at 3, 6, 9, and 12 months revealed that the lesionscovered with membranes healed more quickly than the control lesions. Results of the study indicate that theprinciples of GTR can be effectively applied to the healing of large periapical lesions, especially inthrough-and-through lesions (Figs. 4-10).

One of the main problems in regeneration is bacterial infection. The retrograde filling material should havea good hermetic seal. The resected root surface should be decontaminated to have cemental and periodontalligament regrowth. 19

Another important consideration in regenerative therapy is the interface between the blood clot and theradicular surface: Regeneration needs stabilization and protection of such interface, which is the first

Figure 4. Ferret experiment. Preoperative radiograph, showing through-and-through periapical lesion covered bothbuccally and lingually with Gore-Tex membrane.

Table 2. INDICATIONS FOR GUIDED TISSUE REGENERATION APPLICATION IN ENDODONTIC SURGERY

Through-and-through periapical lesionLarge periapical lesionEndo-perio lesion

Periapical lesion communicating with the alveolar crestFurcation involvement as a result of perforationRoot perforation with bone loss to alveolar crest


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Figure 5. A 3-month postoperative radiograph showing complete periapical bone fil

Figure 6. Preoperative radiograph of tooth number 9, showing through-and-through lesion.


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Figure 7. Gore-Tex membrane placed over lesion.

Figure 8. At 6 weeks later. Re-entry to remove Gore-Tex membrane. A 2-mm by 2-mm trephination is made forhistologic study.


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Figure 9. Histology. Gore-Tex membrane separating soft tissue from bone.

Figure 10. A 3-month postoperative radiograph showing complete bone healing with periodontal ligament space.


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form of attachment leading to new connective tissue attachment. 12 In a clinical situation, the closer thelesion is to the marginal region, the greater the fluids and bacterial contamination from the sulcus and also agreater risk for mechanical trauma. Thus, the combined endodonticperiodontic lesion probably has the leastfavorable prognosis when GTR is used. Combined endo-perio lesions may assume different clinical forms tomicro endo-perio communications.

The adjunctive use of decalcified freeze-dried bone allograft (DFDBA) with ePTFE does not enhance

periodontal attachment over that observed when ePT17E was used alone .6,22 One reason why ePTFE alonemay produce more bone fill than the combination with DFDBA could be that the combination of these twomaterials may create a less ideal environment for wound healing. GTR barriers function by creating a spaceand stabilizing the wound. Addition of DFDBA to the defect may interfere with the space created by thebarrier, thus preventing the repopulation of the site with periodontal ligament cells from the adjacent bone.6DFDBA may inhibit osteoblastic penetration of the site by creating a physical barrier .6,32 Table 3 listsadvantages and disadvantages of GTR in endodontic microsurgery.

CALCIUM SULFATE AS AN ALTERNATIVE TO THEUSE OF BARRIER MEMBRANES IN GUIDED TISSUEREGENERATION APPLIED TO MICROSURGICALENDODONTICS

In the last 3 years, calcium sulfate has been introduced into periodontology and implantology30,31 and inendodontics24 for the treatment of bone lesions. Calcium sulfate was first used in the form of Plaster of Paris,which is a hernihydrate of calcium sulfate .26

Nikulin and Ljubovic23 reported that regeneration of normal bone occurs earlier with calcium sulfate thanwith autogenous grafts. Peltier 26 in 1959 concluded that the hemihydrate of calcium sulfate alone is notosteogenic, but when it comes into contact with periosteurn or bone, regeneration of bone is accelerated.

Bell' in 1960 observed that success of bone grafts depended partially on rapid resorption of the graftmaterial by the host. From his study, calcium sulfate implants were rapidly resorbed, taking an average of 5 to

7 weeks.In 1961, Lebourg and Biouc17 used calcium sulfate to fill extraction sites after surgical removal of impacted molars as well as other osseous defects in the maxilla and mandible. Three to 4 weeks later, theyfound complete resorption of calcium sulfate radiographically and an accelerated healing rate.

Table 3. ADVANTAGES AND DISADVANTAGES OF GUIDED TISSUE REGENERATION IN ENDODONTICMICROSURGERY

AdvantagesBarrier function in case of lack of periosteumGreater concentration of osteogenic cells in the healing areaHigh success rate

DisadvantagesCostPossibility of infectionNeed for a second surgery (nonresorbable materials only)Need for a space-maintaining device in large defects (screw, filling material)Problems in the application of the barrierOperator skill (e.g., high surgical skill required when a palatal flap is raised)


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In 1980, Coetzee8 observed that normal physiologic absorption of calcium sulfate occurred withsimultaneous deposition of autogenous cancellous bone. Calcium sulfate is an *outstanding bone substitute,ensuring bone formation and giving results comparable with autogenous bone, if not better.

In 1984, McKee and Bailey21 concluded that calcium sulfate was replaced by bone in the defects in whichperiosteum was present or in which periosteurn was lost.Indications for calcium sulfate are:

1. Postapicoectomy bone defects.2. Through-and-through lesions.3. Periapical lesions with furcation involvement.4. Postsurgical endo-perio communications.

Calcium sulfate has been demonstrated to perform better as a barrier than membranes.24 Other advantages of calcium sulfate include:

Inexpensive.Ease of application.No inflammatory reaction.Absence of postoperative complications.Possibility of using the material even in a septic environment.Ability to achieve secondary closure of soft tissues on the exposed material.Stabilization of blood clot.Adhesion to root surface.Biocompatible.Complete absorption.

CLINICAL APPLICATION OF CALCIUM SULFATE

Postapicoectomy Bone Defects

It is important to improve the local conditions and enhance the regenerative process in cases in which root isexposed in a bone cavity. Especially in cases in which the bone is thin, connective tissue tends to

Table 4. OPERATIVE PROTOCOL FOR GUIDED TISSUE REGENERATION WITH CALCIUM SULFATE

Root planing of exposed root surfaceRemove granulation tissueHemostasisRinse for 3 min with tetracycline solution

Obturate the defect with calcium sulfate in two stagesPlace the material into the cavity and plug with gauzePlace a second layer of calcium sulfate and close the bony defect slightly in excess


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invade the bone defect quickly, preventing the regeneration of cementum, ligament, and bone. Becausecalcium sulfate has been shown to allow bone regeneration even in the absence of periosteum, along with thebarrier action, an ideal environment can be created for complete healing. Table 4 lists the operative protocolfor GTR with calcium sulfate.

Through-and-Through Lesions

In cases with through-and-through lesions, calcium sulfate has proven to be a better option thanmembranes. First, there is no need to raise a palatal or lingual flap. Second, even in large lesions, thecomplete fill of the cavity, which is undoubtedly contaminated, does not create any problems because calciumsulfate does not undergo necrosis but is washed out by secretions. The operative protocol is the same, but thecalcium sulfate has to be a thick mix, so that resorption takes a longer time. The healing is greatly enhancedwith the use of calcium sulfate, with the radiolucent lesion showing a good degree of bone fill and a morerapid rate of mineralization than normal in just 8 weeks (Figs. 11-16).

Periapical Lesions with Furcation Involvement

The concomitant presence of periapical lesions and furcation lesions creates a problem because theselesions have to be approached simultaneously. GTR in class 11 and Ill furcation lesions has a poor prognosis,and evaluation is difficult. In addition to the standard protocol for the apical lesion, the operative protocolincludes the following:

1. Scale and root plane the furcation lesion.2. Irrigate with tetracycline solution (100 mg/mL).3. Fill the bone defect with autogenous bone and calcium sulfate.4. Place pure calcium sulfate in excess.5. Suture and reposition flap coronally.

The calcium sulfate binds to the bone particles and keeps the graft adherent to the root surface. In addition, if an exposure occurs, infection is limited.


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Figure 11. Preoperative radiograph of tooth number 13 with periapical lesion.

Figure 12. Through and through lesion.


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Figure 13. Immediate postoperative radiograph with root resection, retrograde filling, and calcium sulfate in bonedefect.

Figure 14. 3-month postoperative radiograph showing complete bone fill with PDL space.


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Figure 15. Preoperative radiograph of a ferret experiment. Through-and-through bone defect filled with calciumsulfate and Gore-Tex membrane.

Figure 16. Postoperative radiograph showing defect filled with regenerated bone.


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Postsurgical Endo-Perio Communications

These situations border on whether the tooth should be saved or if implant should be placed. Case selection isimportant, and some of the important considerations for predictable regenerative results are

1. Postsurgical crown-to-root ratio.

2. Mobility.3. Distance of bone landmarks.4. Root curvature.5. Maintenance of an adequate space.6. Vascularity.7. Flap stabilization.8. Osteopromotive potential.

Operative protocol after conditioning the root with tetracycline irrigation is as follows:

1. Mix the autogenous bone particles with calcium sulfate and cover the root with the mixture.2. Trim a Gore-Tex membrane, which is to be secured around the tooth neck (Larnbone [Pacific Coast

Tissue Bank, Los Angeles, CA] membrane may be used as an alternative).3. Position and suture the flap as coronally as possible.4. Emphasize a strict oral hygiene protocol.

The long-term prognosis is questionable in these cases. Bone regrowth can be evaluated by probing,radiographic evaluation, or surgical reentry. Little is known about the relationship between the bone and theunderlying root surface. Even in the case of a single tooth, there is risk of losing more bone, affecting thepossibility of an implant therapy in the future. Prognosis depends on the crown-to-root ratio, the width of thefenestration, and the thickness of the surrounding bone margins. Meticulous treatment planning is of great

importance in these cases.

CONCLUSION

Barrier Membrane Techniques can enhance the quality and quantity of bone regeneration in periapical lesions.Bone growth in circumscribed bone cavities is also accelerated following endodontic microsurgery. The GTRprinciple when effectively applied to the healing of through-andthrough lesions, large periapical lesions, andendo-perio lesions in endodontic surgery can dramatically change the prognosis of the treatment.

References

1. Andreasen JO, Rud J: Mode of healing histologically after endodontic surgery in 70 cases. Int j Oral Surg 1:148-160, 19722. Baek SH, Broome C, Zechner W, et al: Healing of through-and-through osseous defects by membrane barrier technique inferrets. J Endod 21:228, 19953. Bell WH: Resorption characteristics of bone and plaster. Oral Surg 39:727-735, 19604. Boyne P, Lyon H, Miller C: The effects of osseous implant materials on regeneration of alveolar cortex. Oral Surg Oral MedOral Pathol 14:369-378, 19615. Caffesse RG, Nasiieti CE, Morrisson EC, et al: Guided tissue regeneration: Comparison of bioabsorbable andnon-bioabsorbable membranes: Histologic and histometric study in dogs. J Periodontol 65:583-591, 19946. Caffesse RG, Nasjieti CE, Plotzke A, et al: GTR and bone grafts in the treatment of furcations. J Periodontol 64:1145-1153,19937. Cortellini P, Pini Prato Q Tonetti M: Periodontal regeneration of human infrabony defects with bioresorbable membranes: Acontrolled clinical trial. J Periodontol 67:217223,1995

8. Coetzee AS: Regeneration of bone in the presence of calcium sulfate. Arch Otolaryngol 106:405-409, 1980


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VOLUME 41 NUMBER 3 JULY 1997 16 16

9. Dahlin C, Lindhe A, Gottlow J, et al: Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg 81:672-676,198810. Dahlin C, Gottlow J, Lindhe A, et al: Healing of maxillary and mandibular bone defects using a membrane technique. ScandJ Plast Reconstr Hand Surg 24:13-19, 199011. Diggins L, Clay J, Himel V, et al: A combined endodontic retrofill and periodontal GTR technique for the repair of molarendodontic furcation perforation: A case report. Quintess Int 25:109-114, 199412. Garrett S, Bogle C: Periodontal regeneration: A review of flap management. Periodontol 2000 1:100-108, 1993

13. Gottlow J, Laurell L, Rynalder H, et al: Treatment of infrabony defects with bioresorbable and nonresorbable GTR devices[abstr 8231. J Dent Res 72(spec iss):206, 199314. Hjorting-Hansen E, Andreasen J: Incomplete bone healing of experimental cavities in dog mandibles. Br J Oral Surg9:33-40, 197115. Kaban L, Clowacki J: Induced osteogenesis in the repair of experimental mandibular defects in rats. J Dent Res60:1356-1364, 198116. Kaban L, Glowacki J, Murray J: Repair of experimental mandibular defects in rats. Surg Forum 30:519-524, 197917. Lebourg L, Biouc: The imbedding of plaster of Paris in surgical cavities of the jaws. Semin Hop Paris 37:1195-1197, 196118. Lindhe J, Alberins P, Dahlin C, et aE Osteopromotion: A soft tissue exclusion principle using a membrane for bone healingand bone osteogenesis. J Periodontol 64:11161128, 199319. Lowenguth RA, Blieden TM: Periodontal regeneration: Root surface demineralization. Periodontol 2000 1:54-67, 199320. Lundengren D, Nyman S, Mathisen T, et al: Guided bone regeneration of cranial defects, using biodegradable barriers: Anexperimental pilot study in the rabbit. J Craniomaxillofac: Surg 20:257-260, 199221. McKee J, Bailey B: Calcium sulfate as a mandibular implant. Otolaryngol Head Neck Surg 106:405A09, 198422. Mellado JR, Salkin LM, Freedman AL, et al: A comparative study of ePTFE periodontal membranes with and withoutdecalcified freeze-dried bone allografts for the regeneration of interproximal intraosseous defects. J Periodontol 66:751-755,199523. Nikulin A, Ljubovic E: Der Gipsstift in der Experiomentellen Knochenregeneration. Acta Med lugosal 10:1-36, 195624. Pecora G, Andreana S, Margarone J Ill, et al: Bone regeneration with a calcium sulfate barrier. Presented at AmericanAcademy of Periodontology 76th Annual Congress, New Orleans, 199625. Pecora G, Kim S, Celletti R, et al: The guide tissue regeneration principle in endodontic surgery: One year postoperativeresults of large periapical lesions. Int Endod J 28:4146, 199526. Peltier LF: The use of plaster of Paris to fill large defects in bone. Am J Surg 97:331-315, 195927. Rankow HJ, Krasner PR: Endodontic applications of guided tissue regeneration in endodontic surgery. J Endod 22:34-43,1996

28. Rud J, Andreasen JO, Moller-fensen JE: A multivariate analysis of the influence of various factors upon healing afterendodontic surgery. Int J Oral Surg 1:258-271, 197229. Schmitz J, Hollinger J: The critical size defect as an experimental model for craniomandibular nonunions. Clin Orthop205:299-307, 198630. Sottosanti J: Calcium sulfate: An aid to periodontal, implant and restorative therapy. Calif Dent Assoc J 20:45, 199231. Sottosanti J: Calcium sulfate: A biodegradable and biocompatible barrier for guided tissue regeneration. Compend Contin EdDent 13:226-234, 199232. Stahl S, Froum S: Histologic healing responses in human vertical lesions following the use of osseous allografts and barriermembranes. j Clin Periodontol 18:149-152, 1991

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Gabriele Pecora, MDDepartment of Endontics

School of Dental MedicineUniversity of Pennsylvania

4001 Spruce StreetPhiladelphia, PA 19104

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