BARRIER MEMBRANE TECHNIQUES IN ENDODONTIC MICROSURGERY PECORA et al

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

BARRIER MEMBRANE
TECHNIQUES IN ENDODONTIC
MICROSURGERY

Gabriele Pecora, MD, DDS, Seung-Ho Baek, DDS, PhD

Sivakami 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 and
repair. Regeneration is the replacement of destroyed tissue with new tissue formed by the cells of the same
origin. This new tissue reacts in a similar manner against pathologic stimuli. Repair is the restoration of the
tissue destroyed by disease with new tissue consisting of cells different from the original cells. These cells
react differently from the original cells against pathologic stimuli.
One of main concerns in treating an endodontically involved tooth that has a through-and-through osseous
defect is that incomplete bone healing may be inevitable .1, 211 Ingrowth of connective tissue into the
osseous defect prevents periapical bone regeneration. The ingrowth of connective tissue can result in
periapical scarring, which is often misdiagnosed as pathology and may lead to unnecessary surgical reentry by
a practitioner who is not fully aware of the history. When the barrier membranes are placed over bony defects
and 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 defect
time to heal.
Guided tissue regeneration (GTR) is a procedure used to regenerate lost attachment apparatus through
differential tissue response. The objective of GTR in endodontic microsurgery is to enhance the quality and
quantity of bone regeneration in the periapical region and to accelerate bone growth in circumscribed bone
cavities 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 TISSUE

REGENERATION 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 nonresorbable
and 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, polyglactic
acid, 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 or
cellular 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 IN

ENDODONTIC MICROSURGERY

Periapical lesions healing with scar tissue after surgical treatment of periapical granulomas or cysts was
described by Andreason and Rud.1, 111 Histologic changes were studied in 70 biopsy specimens from less
than 1 year to 14 years after endodontic surgery. Healing following periapical surgery can be categorized into
three main types: reformation of the periodontal membrane, fibrous tissue or scar tissue with varying grades
of 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 and
connective 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 numerous
animal 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 further
bone formation. Kaban and Glowacki 16 created 4-mm diameter through-and through defects in the
mandibular 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 defects
exhibited healing with fibrous tissue. Schmitz and Hollinger29 suggested 20-mm defects as the critical size
that would not heal in a monkey mandible.
Dahlin and colleagues9, 111 were the first to apply the concept of GTR to bone surgery, creating the
guided bone regeneration (GBR), or osteopromotion with membrane, and subsequently applied it to
endodontic surgery. In 1988, it was concluded that "the placement of membranes to bony lesions led to a
complete bony restitution of the defects." In 1990, Dahlin and colleagues10 evaluated the healing of maxillary
and mandibular bone defects using the membrane technique in the monkey model. Bilateral transosseous
defects were created in

Table 1. TYPES OF BARRIERS

Resorbable Nonresorbable

Polylactic acid (Guidor, Resolute) PTFE (Gore-Tex)

Polyglactic acid (Vicryl) Rubber dam
Collagen (Biomend, Paroguide, CollaTape)
Fascia
alcium 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 closure
with newly formed bone. A cementum-like tissue, with inserting collagen fibers, was found on the cutting
surface. In the control surgical sites, where no membrane was used, the bone defects were filled with fibrous
connective tissue, characterized by collagen fibers parallel to the root surfaces. Cortical bone did not gain its
continuity 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 surrounding
connective 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 periapical
lesions, and by Rankow and Krasner27 in general to endodontic surgery.
Baek and associates2 evaluated whether improved bone regeneration can be achieved in
through-and-through osseous defects in ferrets with a nondegradable membrane barrier (Gore-Tex) and two
biodegradable 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 or
Guidor membrane (see Fig. 1). The control group, which did not receive any membrane barrier, did not show
any substantial bone regeneration. The Gore-Tex and Vicryl group showed good osteoconductive potential
with almost complete lamellar bone filling. Histologically, bone regeneration in membrane barrier defects
showed 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 suggested
that membrane barrier technique generally improved the bone regeneration in through-and-through periapical
defects.

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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 some
bioresorbable and nonresorbable membranes in periodontology concluded that both membrane types resulted
in clinically and statistically significant improvements in the clinical attachment levels and probing depths. The
use of either of these barriers was equally effective and significantly better than conventional access flaps. It
has been demonstrated that the effectiveness of the biologic principle of the selective repopulation of the
healing wound is independent of the type of barrier material .5

Table 2 lists indications for GTR application in endodontic microsurgery. Some points to remember while
using 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 new
tissue.

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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 were
selected. The lesions had a radiographic diameter of at least 10 mm. They were surgically removed followed
by apicoectomy and retrograde filling with either SuperEBA or desiccated ZOE. In 10 test sites, large
Gore-Tex was used. Radiographic analysis of the lesion at 3, 6, 9, and 12 months revealed that the lesions
covered with membranes healed more quickly than the control lesions. Results of the study indicate that the
principles of GTR can be effectively applied to the healing of large periapical lesions, especially in
through-and-through lesions (Figs. 4-10).
One of the main problems in regeneration is bacterial infection. The retrograde filling material should have
a good hermetic seal. The resected root surface should be decontaminated to have cemental and periodontal
ligament regrowth.19
Another important consideration in regenerative therapy is the interface between the blood clot and the
radicular 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 both
buccally and lingually with Gore-Tex membrane.

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

Through-and-through periapical lesion
Large periapical lesion
Endo-perio lesion
Periapical lesion communicating with the alveolar crest
Furcation involvement as a result of perforation
Root 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 for
histologic 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 the
lesion is to the marginal region, the greater the fluids and bacterial contamination from the sulcus and also a
greater risk for mechanical trauma. Thus, the combined endodonticperiodontic lesion probably has the least
favorable prognosis when GTR is used. Combined endo-perio lesions may assume different clinical forms to
micro 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 alone
may produce more bone fill than the combination with DFDBA could be that the combination of these two
materials may create a less ideal environment for wound healing. GTR barriers function by creating a space
and stabilizing the wound. Addition of DFDBA to the defect may interfere with the space created by the
barrier, thus preventing the repopulation of the site with periodontal ligament cells from the adjacent bone.6
DFDBA may inhibit osteoblastic penetration of the site by creating a physical barrier .6,32 Table 3 lists
advantages and disadvantages of GTR in endodontic microsurgery.

CALCIUM SULFATE AS AN ALTERNATIVE TO THE

USE OF BARRIER MEMBRANES IN GUIDED TISSUE
REGENERATION APPLIED TO MICROSURGICAL
ENDODONTICS

In the last 3 years, calcium sulfate has been introduced into periodontology and implantology30,31 and in
endodontics24 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 than
with autogenous grafts. Peltier 26 in 1959 concluded that the hemihydrate of calcium sulfate alone is not
osteogenic, 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 graft
material 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, they
found complete resorption of calcium sulfate radiographically and an accelerated healing rate.

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

MICROSURGERY
Advantages
Barrier function in case of lack of periosteum
Greater concentration of osteogenic cells in the healing area
High success rate

Disadvantages
Cost
Possibility of infection
Need 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 barrier
Operator 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 with
simultaneous 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 which
periosteum 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 is
exposed 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 surface
Remove granulation tissue
Hemostasis
Rinse for 3 min with tetracycline solution
Obturate the defect with calcium sulfate in two stages
Place the material into the cavity and plug with gauze
Place 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. Because
calcium sulfate has been shown to allow bone regeneration even in the absence of periosteum, along with the
barrier action, an ideal environment can be created for complete healing. Table 4 lists the operative protocol
for GTR with calcium sulfate.

Through-and-Through Lesions

In cases with through-and-through lesions, calcium sulfate has proven to be a better option than
membranes. First, there is no need to raise a palatal or lingual flap. Second, even in large lesions, the
complete fill of the cavity, which is undoubtedly contaminated, does not create any problems because calcium
sulfate does not undergo necrosis but is washed out by secretions. The operative protocol is the same, but the
calcium sulfate has to be a thick mix, so that resorption takes a longer time. The healing is greatly enhanced
with the use of calcium sulfate, with the radiolucent lesion showing a good degree of bone fill and a more
rapid 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 these
lesions 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 protocol
includes 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 bone
defect.

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 calcium
sulfate 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 is
important, 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 the
underlying root surface. Even in the case of a single tooth, there is risk of losing more bone, affecting the
possibility of an implant therapy in the future. Prognosis depends on the crown-to-root ratio, the width of the
fenestration, 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 GTR
principle when effectively applied to the healing of through-andthrough lesions, large periapical lesions, and
endo-perio lesions in endodontic surgery can dramatically change the prognosis of the treatment.

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Address reprint requests to

Gabriele Pecora, MD
Department of Endontics
School of Dental Medicine
University of Pennsylvania
4001 Spruce Street
Philadelphia, PA 19104

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