guided bone regeneration using resorbable and nonresorbable

JOMI on CD-ROM, 1996 Jun (735-742 ): Guided Bone Regeneration Using Resorbable an… Copyrights © 1997 Quinte…

Guided Bone Regeneration Using Resorbable and Nonresorbable Membranes: A Comparative Histologic Study in HumansMassimo Simion, MD, DDS/Antonio Scarano, DDS/Luca Gionso, DDS/Adriano Piattelli, MD, DDS

Resorbable membranes of poly(lactic acid) and poly(glycolic acid) (PLA/PGA) were compared to nonresorbable expanded polytetrafluoroethylene (e-PTFE) membranes in the treatment of defects around titanium dental implants placed in postextraction sockets. Two partially edentulous and three completely edentulous patients requiring implant-supported restorations participated. Sixteen Brånemark implants were placed into extraction sockets and covered with modified titanium cover screws, called harvest cover screws, which allow tissue biopsy at second-stage implant surgery. Seven defects were treated with PLA/PGA membranes, five were treated with e-PTFE membranes, and four were left untreated (control sites). After 6 months of healing, the harvest cover screws were retrieved and processed for light microscopy examination together with the regenerated tissues. Very little or no bone formation was detected in control specimens. The e-PTFE membranes were found to be the most effective barrier material, in that denser and a greater amount of regenerated bone was found. The PLA/PGA membranes produced some bone regeneration when compared to control sites, but to a lesser extent compared to e-PTFE sites.(INT J ORAL MAXILLOFAC IMPLANTS 1996;11:735–742)

Key words: dental implant, expanded polytetrafluoroethylene membrane, guided tissue regeneration, poly(glycolic acid) membrane, poly(lactic acid) membrane

Guided bone regeneration (GBR) techniques have been successfully applied in the treatment of peri-implant bone defects and for increasing the width and height of the alveolar ridge in experimental animals and in humans.1-10 These techniques utilize porous membranes as mechanical barriers to create a secluded space around the defects to permit bone regeneration without the competition of other tissues. The membranes most frequently employed for this purpose are nonresorbable expanded polytetrafloroethylene (e-PTFE). Nonresorbable e-PTFE membranes are supposed to remain in place, completely covered by the soft tissues, for a period of time sufficient to allow bone regeneration and maturation, and then they must be removed with reentry surgery. Most of the osseointegrated implant systems involve a two-stage surgical approach that allows easy removal of the membrane at the second-stage surgery; therefore, reentry procedures are not considered a disadvantage in implant applications. How ever, some advantages could result at


second-stage implant surgery from resorption of the membrane. In fact, absence of the membrane might allow a more limited gingival flap reflection and a partial-thickness flap elevation. Consequently, better adaptation of the gingival tissues to the titanium abutments could be achieved by suturing the flap to the periosteum. Other surgical procedures in the craniomaxillofacial region not requiring two-stage surgery could advantageously use resorbable membranes. These procedures include treatment of bone defects resulting from tumor or large cystic jawbone lesions.

In recent years, a series of investigations has been carried out to study the effectiveness of resorbable poly(lactic acid) (PLA) and poly(glycolic acid) (PGA) membranes in the treatment of periodontal lesions and bone defects in animals.11-13 Poly(lactic acid) and poly(glycolic acid) are α-polyester homopolymers employed as suture material and characterized by a favorable biologic response.11 When the membranes are implanted in the tissues, PLA/PGA membrane resorption generally starts after 4 to 6 weeks, and it is complete after about 8 months.

Cafesse et al12 tested two types of bioabsorbable PLA/PGA membranes in an experimental study on dogs. The membranes were tested for biocompatibility, resorption characteristics, and ability to provide periodontal regeneration; e-PTFE membranes were used as control specimens. It was concluded that from a clinical and histologic point of view, similar results can be achieved in regenerative periodontal surgery using either bioabsorbable or nonbioabsorbable e-PTFE barriers. Sandberg et al13 have shown that PLA/PGA bioabsorbable membranes represent a valid alternative to e-PTFE membranes for improving bone regeneration in standardized defects in rat mandibles, but they indicated that further technical development of the membrane material was necessary.

There is a lack of data relative to the use in hu mans of PLA/PGA membranes as mechanical barriers for guided bone regeneration applications associated with osseointegrated implants. The purpose of the present clinical and histologic study was to evaluate the effectiveness of PLA/PGA membranes in the treatment of bone defects resulting from the placement of titanium implants in postextraction sockets. Similar sites were also treated without membranes and with e-PTFE nonresorbable membranes.

Materials and MethodsPatients. Five patients, aged 44 to 69 years (mean 57.4) and in good general health, participated in the study. Two patients were partially edentulous, and three patients were completely edentulous. All had been referred to the Department of Dentistry, University of Milan, for implant-supported restorations. The extraction of teeth in the sites to be treated was performed 45 to 60 days before the first stage of implant surgery. The gingival tissues were completely healed, but the alveolar sockets were still present at the time of the surgery. The patients were informed that a small biopsy specimen would be taken from the regenerated tissue at the top of the


implants with no untoward effect on implant osseointegration. All the patients volunteered to participate in the study. The study protocol was accepted by the Ethics Committee of the University of Milan.

Surgical Protocol. Implant surgery was performed under local anesthesia (UltracainDS Forte, Hoechst, Frankfurt, Germany) with a sedative premedication (diazepam, 5 mg orally) 30 minutes before surgery. The patients received antibiotic prophylaxis for 7 days (amoxicillin, 1 g, 12 and 2 hours presurgery, and every 12 hours postoperatively) and an anti-imflammatory agent (ketoprofen, 50 mg every 12 hours) for 4 days. A full-thickness crestal incision was made within the keratinized gingiva. Two vertical releasing incisions were made at the distal aspect of the crestal incisions. When postextraction sites to be treated with implants were adjacent to residual teeth, the crestal incision was extended intrasulcularly one tooth farther before making the vertical releasing incision. The flaps were gently reflected buccally and lingually with a periosteal elevator, taking care to not damage the periosteum and to minimize soft tissue trauma. The residual postextraction bone defects were carefully debrided and curetted to remove all soft tissues.

A total of sixteen Brånemark implants (Nobel Biocare AB, Göteborg, Sweden) were placed into extraction sockets in the maxilla and in the mandible according to the standard procedure described by Adell et al.14 Standard 3.75-mm-diameter implants with lengths between 10 and 15 mm were used. Primary stabilization was achieved by anchoring the implants in the normal bone present apically to residual alveolar sockets. The implant recipient sites were not pretapped to improve primary stabilization.

After placement, instead of covering the implants with the standard cover screws, modified commercially pure titanium baskets called harvest cover screws (HCSs) (Fig 1) were applied to the top of the implants according to the technique described previously15 (Fig 2). The HCSs are 4 mm in diameter and 2 mm in height, and they are designed to allow harvesting of the tissue regenerated on top and into the hollow of the basket at the time of second-stage surgery. The implants were positioned so that the upper rims of the HCSs were at the level of the alveolar crest or 1 mm below. In this way, angular bone defects of different sizes resulted around the implants and the HCSs.

Membranes. Seven sites were covered with PLA/PGA membranes (Resolut, WL Gore, Flagstaff, AZ), five sites were treated with e-PTFE membranes (GTAM, WL Gore), and four sites were left untreated (control sites). The distribution of the site treatment in each patient was randomly determined. Each membrane was stabilized at the buccal edge with a stainless steel fixation screw (Memfix, Straumann, Waldenburg, Switzerland) (Fig 3). The flaps were closed with vertical mattress sutures alternating with interrupted nonresorbable sutures (WL Gore). Postoperatively, chlorhexidine rinses (Corsodyl, ICI Pharmaceuticals, Macclesfield, Cheshire, England; 0.2% solution twice a day) were prescribed for the patients for 2


weeks. Patients were not allowed to wear provisional removable prostheses for a minimum of 15 days to avoid pressure on the wound area. The sutures were removed after 10 days. The patients were checked once a week for the first month and then once a month until second-stage surgery.

Reentry. Second-stage surgery was performed after 6 months of healing. Surgical areas were reopened with a midcrestal, full-thickness incision, and buccal and lingual flaps were reflected. The HCSs, together with the overlying newly formed tissue and membranes, were removed en bloc through careful dissection from the adjacent tissues with a fissure bur. The specimens were processed for histologic analysis.

Histologic Examination. The HCSs and surrounding tissues were washed in saline solution and were immediately fixed in 4% paraformaldehyde and 0.1% glutaraldehyde in 0.15 mol/L cacodylate buffer at 4°C and pH 7.4, to be processed for histology. The specimens were processed to obtain thin ground sections with the Precise 1 Automated System (Precise, Pescara, Italy). The specimens were dehydrated in ascending series of alcohol rinses and were embedded in a glyco(methyl methacrylate) resin (Technovit 7200 VLC, Kulzer, Wehrheim, Germany). After polymerization, the specimens were sectioned with a high-precision diamond disk at about 150 mm and were ground to about 30 mm. The slides were stained with acid fuchsin and toluidine blue. Von Kossa staining was also done to visualize the calcified structures. After polishing, the slides were immersed in silver nitrate for 30 minutes and were exposed to sunlight. Then the slides were washed under tap water, and they were dried and mounted. For the enzyme histologic staining of alkaline and acid phosphatase, the protocol has been described previously.16

Two histologic sections were obtained from each specimen. The sections were evaluated by two independent examiners unaware of the specimen treatment. The examiners evaluated the presence of bone in the space inside the HCS using conventional (– and + to +++) score values (– indicates absence of bone; + bone present in one third of the space inside the HCS; ++ bone present in two thirds of the space inside the HCS; +++ bone completely fills the space inside the HCS).

ResultsClinical Findings. The healing period was uneventful in all sites. All patients recovered well, and no signs of infection were detectable. In two sites, a dehiscence of the membrane occurred after 10 to 20 days of healing. The dehiscences involved a PLA/PGA membrane in one patient and an e-PTFE membrane in the other. They were treated twice a day with topical applications of chlorhexidine gel (0.2% Corsodyl Gel, ICI Pharmaceuticals). The exposed PLA/PGA membrane demonstrated progressive resorption and completely disappeared after 4 weeks of exposure to the oral cavity. Subsequently the soft tissues healed spontaneously without any residual clinical sign of inflammation. The exposed e-PTFE membrane


was maintained for 1 month with chlorhexidine applications, and then it was removed. The remaining 14 sites remained covered by the soft tissues until the second-stage surgery after 6 months.

At the reopening, all implant sites showed healthy gingival tissues. The e-PTFE membranes appeared to be firmly adherent to the underlying newly formed tissue, and no clinical signs of inflammation were evident. The PLA/PGA membranes were not macroscopically recognizable, and only the fixation screws appeared to have been placed directly in the alveolar bone (Fig 4).

Histologic Findings. The scores for the newly formed bone reported by the examiners are shown in Table 1.

Expanded Polytetrafluoroethylene Membranes. Histologic analysis revealed new bone formation inside and on top of all the HCSs treated with nonexposed e-PTFE membranes (Fig 5a). The site at which the e-PTFE membrane dehisced and was removed did not show any bone formation in the HCS. The specimens treated with e-PTFE demonstrated a greater amount of regenerated bone, and this bone was also denser when compared to PLA/PGA specimens. The newly formed bone appeared mature and compact in the central portions of the HCSs. In contrast, in the most peripheral areas close to the membrane surface, the bone had the tendency to appear immature with wide osteocytic lacunae and with osteoblasts lining its peripheral border (Fig 5b). Histochemical staining for alkaline and acid phosphatase was negative. In most specimens, the bone was separated from the membrane surface by a thin layer of dense connective tissue with scattered fibroblasts and fibrocytes. Only small areas of the membrane were in contact with the bone without the interposition of connective tissue. In one instance, some bone formation was detectable on the external surface of the membrane.

All of the specimens treated with e-PTFE showed areas of direct contact between the newly formed bone and the HCS titanium surface (Fig 5c). In areas where the bone was not in contact with the titanium surface, a continuous layer of loose connective tissue was present. This tissue, in some instances, exhibited areas of ongoing mineralization with a continuous layer of osteoid tissue lining the implant surface. Many specimens showed artifacts, and a visible empty space was interposed between bone and the titanium surface. These artifacts were presumably the result of retrieval procedures or to the cutting and grinding processes.

Poly(lactic acid) and Poly(glycolic acid) Mem branes. In all of the specimens treated with PLA/ PGA membranes, it was impossible to detect any remnant of the membrane. Inflammatory cells were absent in all specimens of this group. Bone formation was present in all of the specimens inside the HCSs, except the one in which the membrane showed early exposure to the oral cavity. However, in all PLA/PGA treated sites, the quantity of bone appeared to be less than that in the sites treated with e-PTFE membranes. The newly formed bone had a tendency to be


localized in the peripheral areas of HCSs; in all specimens but one, it was absent in the central areas close to the HCS fixation screws (Fig 6a). In three of seven specimens, new bone formation was detectable in only one third of the space inside the HCS. One specimen showed half of the space filled with new bone, and one was completely filled. The spaces void of bone were filled with dense, fibrous connective tissue with few cells and capillaries (Fig 6b). The bone appeared compact and mature with narrow osteocytic lacunae and arrangement of osteons with many haversian canals.

The newly formed bone was in direct contact with the HCS titanium surface, even though some artifacts from retrieval surgery and from the cutting and grinding process were also noticeable in this group (Fig 6c). For this reason, no histomorphometric measurements related to the percentage of direct bone-titanium contact were made.

In two specimens, it was possible to observe osteoblasts arranged in an osteoblastic rim. However, their morphology was that of inactive cells, and apparently, they were not laying down bone matrix. The histochemical staining for alkaline and acid phosphatases was negative. The HCS corresponding to the early exposed PLA/PGA membrane was filled with dense fibrous connective tissue without inflammatory infiltrate.

Control Specimens. The control specimens showed small layers of bone formation in the most peripheral areas of the HCSs. The central areas were colonized by fibrous connective tissue completely surrounding the HCS fixation screws (Fig 7). In few and limited areas, it was possible to observe bone not yet mineralized.

DiscussionThe present controlled clinical and histologic study compares PLA/PGA resorbable membranes with nonresorbable e-PTFE membranes concerning their capability for promoting bone regeneration around titanium implants placed in recent extraction sockets in humans. Modified titanium cover screws, the harvest cover screws, were used to collect tissue samples at second-stage implant surgery. In an earlier study15 this experimental model was found to be an effective method for obtaining tissue biopsy specimens from titanium dental implants without damage to implant function and injury to the patient.

Results of the present study clearly demonstrated a positive effect of barrier membranes on bone regeneration around implants placed in postextraction sockets. Very little or no bone formation was detected in the control specimens. This finding confirms earlier studies,5,15,17,18 which demonstrated that the periosteum alone has scarce osteogenic potential in adult animals and humans.

The group of specimens treated with nonresorbable e-PTFE membranes demonstrated the larger amount of bone formation. In the present study, the amount


of bone regeneration obtained with e-PTFE membranes was significantly higher than that observed in a study15 with the same experimental design. The possible explanation for this finding could be an augmented height of the HCS fixation screws in this study model. By protruding from the HCS baskets, the fixation screws could have acted as tent poles for the prevention of membrane collapse, thus augmenting the space for bone regeneration. Studies by Dahlin et al1,5,18 have demonstrated that the amount of bone regeneration is determined and limited by the available space.

The specimens treated with PLA/PGA membrane showed some bone regeneration into and over the HCSs, but the amount of newly formed bone was visibly less than that seen in the specimens treated with e-PTFE. Two factors could have influenced the quantity of bone formation: the space-maintaining capability and its duration; and the lasting of the barrier effect of PLA/PGA membranes. The stiffness of the resorbable material used in the present study was not sufficient to guarantee the maintenance of an adequate space between the membrane and the defect, without using appropriate grafting materials as space holders. Moreover, the space maintaining capability could potentially decrease with the progression of membrane resorption. This is in accordance with the findings of Sandberg et al,13 who noted that some resorbable membranes used in their study showed lack of stiffness, resulting in a collapse of the membrane into the defect area, causing the newly formed bone to take on an hourglass shape.

The PLA/PGA membranes used in the present study generally started to resorb after 4 to 6 weeks, and resorption was complete after about 8 months postimplantation. With membrane resorption, the barrier effect could decrease too soon to achieve complete bone regeneration. The importance of a long-lasting barrier effect has been demonstrated by Lekholm et al19 in an experimental study on dogs, in which they observed that premature membrane removal reduced the amount of bone regeneration.

Regarding the use of resorbable membranes in guided tissue regeneration procedures, results from the present study indicate some differences between periodontal and bone applications relative to the timing of membrane resorption. In periodontal applications, the critical period appears to be 3 to 4 weeks after first-stage surgery.12,20,21 This period is necessary to allow complete repopulation of the affected root by the selected progenitor cells located in the adjacent healthy periodontal ligament. Results from the present study, together with the results from the Lekholm et al study,19 seem to indicate that a longer barrier effect may be necessary for complete population of the defect by osteogenic cells. Therefore, to achieve complete regeneration, it may be necessary to use PLA/PGA resorbable membranes in association with osteoconductive/osteoinductive space-maintaining material, such as autogenous bone grafts. Another possibility might be that resorbable membranes could be manufactured with reinforcing resorbable structures13


13 in such a way that the membrane could maintain its stiffness and thus its barrier effect for a longer period of time.

The absence of bone formation in the two sites where the membrane dehisced during the early healing period confirms the results of other studies.22-24 These studies have demonstrated that early exposure of the membrane, with consequent bacterial contamination of the healing tissues, hinders bone regeneration, despite careful maintenance with chlorhexidine applications. In a recent study in vitro, Simion et al25 demonstrated that exposure of PLA/PGA resorbable membranes to the oral cavity resulted in complete resorption after 3 to 4 weeks. This is in accordance with the clinical observations of the present study, in which the dehisced PLA/PGA membrane progressively resorbed, with consequent spontaneous healing of the soft tissues without any residual sign of inflammation after 4 weeks. This particular behavior could be considered an advantage because spontaneous healing and closure of the dehisced tissues reduces the time of maintenance of the exposed membrane and avoids membrane removal surgery. On the other hand, a too-precocious resorption may hinder the barrier effect and the space-maintaining ability of the membrane, thereby compromising bone regeneration. Histologic observation of the absence of bone formation in the HCS corresponding to the exposed PLA/PGA membrane seems to support this hypothesis.

In all specimens, it was possible to observe a limited number of osteoblasts. They appeared inactive, and the histochemical staining for alkaline and acid phosphatases was negative. This can probably be explained by the fact that the specimens were retrieved 6 months after implant placement when the bone forming activity was already strongly reduced. This explanation can be substantiated by a recent study16 on rabbits, in which it was possible to demonstrate a very high alkaline phosphatase activity in the bone tissue around titanium implants during the first 3 to 4 weeks after implantation, and a sharp decline of this activity from the fourth week onward.

Results from the present study should be regarded with caution because standardized bone defects could not be produced in humans for obvious ethical reasons. Consequently, precise histomorphometric evaluations could not be done. Moreover, minor differences in coronoapical position of the implant-HCS unit may have introduced some minor variation in the results.

ConclusionWithin the limits of the present study, the results have confirmed in humans that guided bone regeneration techniques are capable of producing new bone osseointegrated with titanium dental implants. Among the barrier materials tested, nonresorbable e-PTFE membranes were shown to be the most effective because they provided the denser and greater amount of bone regeneration. The PLA/PGA resorbable membranes have been shown to produce some bone regeneration when compared to control sites, but to a lesser extent when compared to e-PTFE treated


sites.

AcknowledgmentsThe authors would like to thank Prof A. Salvato and the staff at the Department

of Dentistry, University of Milan, San Raffaele Hospital, for making this study possible.


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Fig. 1 Harvest cover screw (HCS) components: complete HCS (left); pure titanium basket (center); and fixation screw ( right). Each HCS is 4 mm in diameter and 2 mm in height.

Fig. 2 Harvest cover screws in the implant sites. Each implant has been positioned so that the upper rim of the HCS is at the level of the alveolar crest. Angular bone defects of different sizes result around the implant and the HCS.

Fig. 3 The PLA/PGA (left) and e-PTFE (right) membranes have been positioned and stabilized with Memfix miniscrews placed at the buccal edge of the membrane. The membranes are adapted to the bone crest before suturing with vertical mattress sutures. The control site (center) has been left untreated.


Fig. 4 Second-stage surgery after 6 months of healing. The e-PTFE membrane appears to be firmly adherent to the underlying newly formed tissue, and no clinical signs of inflammation are evident. The PLA/PGA membrane is no longer macroscopically recognizable.

Fig. 5a Harvest cover screw treated with e-PTFE membrane. Complete new bone formation is evident inside and on top of the HCS (toluidine blue and acid fuchsin stains; original magnification × 12).


Fig. 5b Same specimen as in Fig 5a, but at a higher magnification. The more peripheral areas close to the membrane surface are seen (large open arrows). Newly formed bone appears immature with wide osteocytic lacunae (small black arrows) and with osteoblasts lining its peripheral border (large black arrows) (toluidine blue and acid fuchsin stains; original magnification × 200).

Fig. 5c Specimen treated with e-PTFE. Areas of direct contact between the newly formed bone and the HCS titanium surface are revealed (toluidine blue and acid fuchsin stains; original magnification × 16).


Fig. 6a Harvest cover screw treated with PLA/PGA membrane. The newly formed bone is localized in the peripheral areas of HCS but absent in the central area close to the HCS fixation screw (toluidine blue and acid fuchsin stains; original magnification × 16).

Fig. 6b Harvest cover screw treated with PLA/PGA membrane. In this specimen, new bone formation is detectable in only one third of the space inside the HCS; the remaining space is filled with dense and fibrous connective tissue with few cells and capillaries (toluidine blue and acid fuchsin stains; original magnification × 12).


Fig. 6c Higher magnification of HCS treated with PLA/PGA membrane. Direct contact between the newly formed bone and the titanium surface is evident (toluidine blue and acid fuchsin stains; original magnification × 50).

Fig. 7 Harvest cover screw with no membrane (control). Bone is limited to the external areas of the HCS. The central area is colonized by fibrous connective tissue completely surrounding the HCS fixation screw (toluidine blue and basic fuchsin stains; original magnification × 12).

guided bone regeneration using resorbable and nonresorbable

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