703
Guided Tissue Regeneration for Implants Placed Into Extraction Sockets: A Study in Dogs William Becker, * Burton E. Becker, * Mark Handelsman,T Tomas Albrektssons
Twelve 10
Clifford Ochsenbein,* and
placed into immediate extraction sockets in dogs. Six PTFE isolated with membranes and 6 sites served as controls. Standardized implants clinical measurements were taken at test and control sites. At 18 weeks the dogs were anesthetized and flaps were laid for the purpose of obtaining clinical measurements. The average gain of bone around augmented implants was 2.6 mm, while control sites had an average bone gain of 1.0 mm. Ridge width adjacent to augmented sites increased by 1.2 mm and control sites had an increased width of 0.6 mm. Histologie evaluation of test and control specimens showed greater bone formation around augmented implants. Implants augmented with PTFE membranes had clinically significant amounts of bone regeneration when compared with controls. / Periodontol 1991; 62:703-709. mm implants were
were
Key Words: Bone regeneration; Osteogenesis; dental implants.
predictability of dental implants to integrate with the surrounding bone has provided the means to restore function to patients who are totally or partially edentulous.1'2 Recently the principle of guided tissue regeneration (GTR) has been applied to dental implants. Membranes are used to create a space and to protect the blood clot over implants in order to preferentially allow bone to grow into the space. Dahlin et al.3 created dehiscence defects over implants placed into the femur of rabbits. Test sites were protected by polytetrafluorethylene (PTFE) membranes, while control sites were unprotected. The membranes were used to prohibit connective tissue from contacting dehisced implant surfaces. At retrieval test sites had an average gain of 3.8 mm of new bone, while control sites had an average gain of 2.2 mm. Becker et al.4 removed P2, P3, and P4 10 weeks prior to implant placement. Implants were placed into the mandible of dogs. Dehiscence defects were created over the labial surfaces of the implants. Test sites were protected by implant augmentation material, while unprotected sites served as controls. Eighteen weeks after initial surgery the sites The
'University of Southern California, School of Dentistry, Los Angeles, CA; University of Texas, School of Dentistry, Department of Periodontics, Houston, TX; private practice, Tucson, AZ. •University of Texas, School of Dentistry, Department of Periodontics, Houston, TX; private practice, Tucson, AZ. •University of Southern California, School of Dentistry, Los Angeles, CA. 'Private practice, Dallas, TX. "Department of Handicapped Research, Goteborg, Sweden.
measured and the implants and surrounding bone were retrieved for histologie evaluation. At 18 weeks the test sites measured an average of 1.38 mm of coronal bone growth, while the control sites had an average of 0.23 mm of new bone. Histologie evaluation demonstrated osseointegration of test and control specimens. Test sites had more bone regeneration and fewer exposed threads when compared with the control specimens. Zablotsky et al.5 removed mandibular posterior teeth in dogs and allowed 12 weeks for healing prior to implant placement. At implant placement, the sites were prepared and prior to placement, dehiscences were produced in the facial alveolar bone. The implants were then placed. PTFE membranes were used to isolate the dehisced hydroxyapatite-coated and titanium implants in dogs. Half of the implants were protected by membranes and the other half served as unprotected controls. The HA-coated PTFE protected implants had an average of 95.17% bone regeneration, while the grit-blasted titanium test implants had 82.8% bone regeneration. The HA-coated control implants had an average of 55% bone regeneration and the titanium implants had an average of 39% bone fill. There may be advantages to placing implants into extraction sockets and protecting them with membranes. Immediate placement of implants into extraction sockets may protect the ridge from resorbing. If ridge height and width can be preserved, longer implants can be placed, thereby increasing the bone volume contacting the implant. Furthermore, immediate implant placement into extraction sites were
704
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
may shorten the time necessary to complete the restorative phase of treatment. It is the purpose of this study to evaluate bone regeneration around implants placed into immediate extraction sockets and protected by implant augmentation material. An immediately-placed implant is defined as an implant placed at the time of tooth extraction. The study will also evaluate the effect of membrane placement on ridge width. Non-membrane treated implant sites will serve as controls.
MATERIALS AND METHODS Three large hound dogs were used for this study. Three weeks prior to the study the animals were anesthetized with Ace promazine and P3 was removed from each of the dogs. The purpose for removing these teeth was to provide adequate flap access during implant placement. Two weeks prior to initiating this study, the dogs' teeth were scaled and polished. One week prior to the study, the dogs' teeth were brushed with Chlorhexidine. The animals were anesthetized with Ace promazine and maintained with nitrous oxide. For anatomic reasons implants were placed in the mandible. Appropriate infiltration anesthesia was administered and P2 and P4 were removed. Test and control sites were chosen by coin flip. After the first test and control sites were chosen, the sites were alternated for the opposite side of the jaw. Mid-crestal incisions were made from the furcation of PI to the mesial aspect of P5. In order to achieve adequate surgical access, short vertical releasing incisions were made at the anterior and posterior aspects of the flaps. Number 10 round acrylic burs under a constant stream of sterile saline were used to enlarge the occlusal aspect of the extraction socket and to create dehiscence defects on the buccal aspect. The sites were prepared as described by Adell6 and 10 mm standard Branemark implants1 were installed in test and control sites. The implants were placed in such a manner that 2 to 4 threads were exposed on the buccal aspect. If a sufficient number of threads was not exposed, a small chisel was used to remove bone from the buccal implant surface. All implants were immobile at the time of placement. Measurements were made with a standardized Williams probe. Photographic documentation was made at the time the measurements were taken and for all surgical steps. Mid-buccal measurements were made from the top of the implant cylinder to the apex of the dehiscence. The width of the defect at the apical and coronal aspects of the dehiscences was also measured. Implant augmentation material* was adjusted to cover the dehiscence and extended over the adjacent bone by 3 to 5 mm in all directions. The augmentation material is manufactured from expanded PTFE and has an outer partially occlusive weave and an inner relatively occlusive design. A rubber dam punch was used to place a small hole in the material. The implant cover screw secured the material to
'Nobelpharma USA, Chicago, IL. #W.L. Gore and Associates, Flagstaff, AZ.
the implant. The width of the alveolar ridge was measured with a 6.5 cm implant caliper.** Buccal-lingual measurements were taken 1 to 2 mm within the lateral borders of the material and one measurement was taken at the midbuccal implant aspect. The surgical area was rinsed and the flaps were sutured with interrupted 4-0 Dexon sutures. The animals were placed on the antibiotic Tribrissen (30 mg/ kg) orally for 7 days and the surgical areas were inspected weekly. At this time the teeth were polished with Chlorhexidine and saline. The dogs were examined bimonthly. At this examination the surgical areas were evaluated for exposure of cover screws or augmentation material and the teeth were polished with Chlorhexidine. If the material became exposed, it was removed between 14 and 20 days after exposure and the material retrieval incisions were resutured. Eighteen weeks post-implant insertion the animals were anesthetized and the areas of surgery were examined and photographed. Mid-crestal incisions were made and buccal-lingual flaps were reflected exposing the implant sites. Photographs were taken. All implants were immobile. Sites which received membranes had clinically evident increases in ridge width. The membranes were firmly adherent to the underlying bone and had to be separated from the bone by sharp dissection. After membrane removal, mid-buccal measurements were taken from the top of the cylinder to the level of alveolar bone. Three measurements were made of the buccal-lingual alveolar ridge width adjacent to the implants. These measurements were averaged and compared with the initial buccal-lingual measurements. The animals were sacrificed, x-rays were taken, and the specimens were removed from the mandibles. Block specimens were fixed in 4% neutral formalin. The specimens were dehydrated and embedded in methyl methacrylate as described by Donath et al.7 Sections were made through the implants and the surrounding undecalcified bone. After grinding the primary sections to a thickness of 10 to 15 µ , they were stained with 1% toluidine blue in a 1% Borax solution mixed in proportions of 4 to 1 with a 1% pyronin-G solution. The interfacial tissue reactions were studied in a Leitz light microscope connected to a Microvid system and an IBM computer. All histologie analyses were performed in a blind manner and the examiner did not know whether he was observing a test or control specimen. RESULTS During the 18-week healing interval, augmentation material became exposed at 4 test sites, while cover screws became exposed at 2 control sites. The material at the test sites became exposed at 12, 19, 27, and 41 days postsurgery, while control cover screws became exposed at 12 and 14 days. The areas of material exposure were examined for inflammation and infection on a weekly basis. Material which became exposed was arbitrarily removed between 14 and **Ace
Dental, Boston, MA.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
Table 1. Mid-Buccal
(in mm)
Subject No.
Site
(PE) (PE) (TO)* (TO)* (BL)* (BL)* mean
s.d.
R L R L R L
Changes
in Bone
Height for Test and
Controls
Tests Exam Exam Exam 2 1 Difference 1 4.0 0.0 4.0 3.0 5.0 0.0 5.0 4.0 3.5 2.0 1.5 3.0 6.0 3.0 3.0 5.0 1.0 6.0 4.0 3.0 4.0 2.5 1.5 4.0
Control Exam 2 Difference
2.0 4.0
0.0 1.0 1.0 0.0 4.0 0.0
4.4 0.92
3.2 1.17
1.0 1.55
1.8 1.41
2.7 1.60
4.2 1.17
3.0 3.0 2.0 5.0
705
All data rounded to nearest decimal; 6; R right; L left. *Sites where material became exposed and was removed. =
=
=
Figure 2. Augmentation material was secured to the implant with the cover screw.
Figure
1.
days
Implants have been placed into immediate extraction sockets.
after exposure. Due to the small sample size, it was not possible to establish a relationship between early membrane removal and increases in bone height (Table 1). The 2 test sites where the material remained unexposed had complete bone regeneration, while the remaining 4 test sites had slight residual areas of thread exposure. When there was exposure of material or cover screws, the exposure was always along the suture line. At 18 weeks the soft tissues adjacent to the implants were relatively uninflamed and all implants were stable. Clinical changes in bone for augmented and control implants can be seen in Figures 1, 2, 3, 4A, and 4B. Changes in mid-implant bone height can be seen in Table 1. The average initial mid-buccal bone height for material augmented sites was 4.4 mm. At retrieval the mean mid implant bone height was 1.8 mm. The average change in bone level for the material augmented sites was 2.6 mm. For controls, the initial mean mid-buccal bone height was 4.2 mm, while at 18 weeks the mean mid-buccal bone level was 3.2 mm. There was a gain of 1 mm. Changes in alveolar ridge width can be seen in Table 2. The average width of the alveolus adjacent to the augmented implants at insertion was 8.1 mm. At 18 weeks the mean alveolar ridge width was 9.2 mm. There was an in-
21
Figure 3. Exposure of implants 18 weeks after initial surgery. Note minimal bone formation adjacent to control implant. The augmentation has remained in position for the entire healing time.
Figure 4A. The augmentation material has been derlying bone. Note increase in bone width. crease
in
dissected from the
ridge width for all material augmented sites.
un-
For
controls, the mean initial alveolar ridge width was 8.5 mm.
At 18 weeks the average alveolar
ridge width was 8.9 mm.
706
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
All data rounded to nearest decimal; 6; R right; L *Sites where material became exposed and was removed. =
=
=
left.
Histological examinations verified the general clinical findings of more bone being present adjacent to membranetreated implants when compared with controls. A statistical comparison could not be performed, as it was difficult to precisely match peripheral sections with corresponding test and controls. In the central sections, cut in the long axis of the specimens, matching was easier; however, the impact of bone growth in this region was most likely not related to membrane placement. When control and test implants were examined histologically, there was generally more bone adjacent to membrane treated implants (Figs. 5A and 5B). Figure 6 demonstrates a specimen with the augmentation material in place. There is mature bone directly beneath the material. In most test sites there were points of direct bone to implant contact (Fig. 7A), while control specimens usually had a soft tissue layer between the implant and bone (Figs. 7B and 7C). In Figure 8A there is a specimen with a retained portion of the membrane. There is profuse new bone formation, with a continuous thin layer of soft tissue separating the membrane from the underlying bone. Figure 8B demonstrates minimal soft tissue inflammation between the membrane and new bone.
FiS"re 5A- Control specimen. marked by an asterisk
Note absence
of bone over threads.
Area
DISCUSSION This study provides preliminary evidence that implants placed into fresh extraction sockets and augmented with PTFE membranes have a greater amount of bone regeneration when compared with unprotected controls. Similarly, ridge width increased adjacent to sites which were augmented with membranes, while non-augmented sites had clinically insignificant increases in ridge width. It is important to
point
out that ridge width measurements were not taken from standardized points and consequently there is a high probability of measurement error. Recognizing that the sample size and increases in ridge width are small, nonetheless, there was an increase in ridge width at each test site. For controls, there were 2 sites which had an increase in ridge width. The trend for augmented sites to have an increase in ridge width might have been more significantly demonstrated with an increase in sample size. It is interesting to note that the material was prematurely removed due to exposure on 4 out of 6 test sites. Due to the small sample size, it was not possible to establish a relationship between premature material removal and increases in bone height. We are presently evaluating this relationship and will be reporting our results in the future.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
707
Figure 5B. Augmented test site demonstrates almost complete formation of new bone over previously exposed threads. New bone marked with circled asterisk.
Figure IB. (arrows). Figure 6. Test site with membrane still in place (arrows). Note vital bone tissue beneath membrane. Bt
=
bone tissue. Ti
=
titanium.
The clinical evidence of bone regeneration was substantiated to a lesser degree by the histologie data. There were 12 possible specimens which could be examined (6 test, 6 controls). There was a tendency for augmented specimens
Control specimen
demonstrating an interfacial thin white line
compared to control sites. Lack of definitive histologie evidence of significant differences between test and control specimens may be related to processing errors. If the specimens were sectioned tangentially rather than perpendicular to the mid-buccal plane, the area of clinical interest might have been missed. Barzilay et al.8 placed an implant into an extraction socket of to have less thread exposure when
708
Figure 8B. Arrows pointing to soft tissue Asterisk is portion of retained membrane.
7C. Control specimen with and bone (asterisks).
Figure
soft
tissue
interface
between
implant
Figure 8A. New bone formation directly beneath the retained membrane surface (asterisk over membrane). The bone was lamellarized.
monkey. The implant was loaded for 6 months. The implant was removed in block and the implant was in contact with bone 58.2% of the implant length. The purpose of placing augmentation material over implants placed into extraction sites is to provide a space for blood clot retention and organization. By excluding flap a
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
lining beneath
the membrane.
epithelium and connective tissue, bone can preferentially be allowed to fill the membrane protected space. When placing implants into extraction sites it is important to prevent fibrous tissue from growing between the implant and the adjacent bone defect. If fibrous tissue grows into the defect the possibility for bone ingrowth will be diminished. Histologie examination of membrane-augmented implants demonstrated active bone formation immediately beneath the membrane. Other specimens demonstrated greater bone contact with augmented implants when compared with controls, and generally there was greater bone adjacent to membrane augmented implants. Lazzara9 placed PTFE membranes over implants which were placed into extraction sockets. The membranes were removed between 4 and 6 weeks after surgery. At the second stage procedure there appeared to be varying amounts of bone around the membrane protected implants. Nyman et al.10 reported 2 cases where membranes were used for implants. One implant was placed into an extraction socket and protected by a PTFE membrane. The membrane was removed at the second stage procedure and clinical and radiographie evidence of bone formation was evident around the augmented implant. Becker et al.11 recently reported a surgical technique for attaining flap closure for implants placed into extraction sockets and augmented with PTFE membranes. At the second stage, there was clinical evidence of bone formation around the augmented implants. Clinical trials are currently being performed for the purpose of evaluating the use of augmentation material over implants placed into extraction sockets. CONCLUSION The present study presents evidence that the principles of guided tissue regeneration can be applied to implants placed into fresh extraction sockets which are augmented by membranes. While this study was performed in dogs, there is reasonable evidence to support testing these principles in clinical trials.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
Acknowledgments
study was supported by W.L. Gore and Associates. Implant equipment was supplied by Nobelpharma, USA.
This
REFERENCES 1. Albrektsson , Dahl E, Enbom L, et al. Osseointegrated oral implants. A Swedish multicenter study of 8139 œnsecutively inserted Nobelpharma implants. / Periodontol 1988; 59:287. 2. van Steenberghe D, Lekholm U, Bolender C, et al. The applicability of osseointegrated implants in the rehabilitation of partial edentulism: A prospective multicenter study on 558 fixtures. IntJ Oral Maxillofac Implants 1990; 5:272. 3. Dahlin C, Sennerby L, Lekholm U, Linde A, Nyman S. Generation of new bone around titanium implants: An experimental study in rabbits. IntJ Oral Maxillofac Implants 1989; 4:19. 4. Becker W, Becker BE, Handlesman M, et al. Bone formation at dehisced dental implant sites treated with implant augmentation material: A pilot study in dogs. Int J Periodontics Restorative Dent 1990; 10:93. 5. Zablotsky M, Meffert R, Caudill R, Evans G. Histological and clinical comparisons of guided tissue regeneration on dehisced HA-coated
6.
7.
8.
9.
10.
11.
709
and titanium endosseous implant surfaces. A pilot study. Int J Oral Maxilo Implants In press. Adell R, Lekholm U, Branemark P-I. A 15 year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981; 10:87. Donath , Breuner G-A. A method for the study of undecalcified bones and teeth with attached soft tissue. The Saege-Schliff technique. J Oral Pathol 1982; ll:d318. Barzilay I, Graser JGN, Caton J, Shenkle G. Immediate implantation of pure titanium implants into extraction sockets. / Dent Res 1988; 67 (Spec. Issue):234 (Abstr. 234). Lazzara RJ. Immediate implant placement into extraction sites: Surgical and restorative advantages. Int J Periodontics Restorative Dent 1989; 9:333. Nyman S, Lang NP, Buser D, Bragge U. Bone regeneration adjacent to titanium dental implants using guided tissue regeneration: A report of two cases. Int J Oral Maxillofac Implants 1990; 5:9. Becker W, Becker BE. Guided tissue regeneration for implants placed into extraction sockets and for implant dehiscences: Surgical techniques and case reports. Int J Periodontics Restorative Dent 1990; 10:377.
Send
reprint requests to: Dr. William Becker, 801 North Wilmot, Tuc-
son, AZ 85711.
Accepted for publication June 21,
1991.
Guided Tissue Regeneration for Implants Placed Into Extraction Sockets: A Study in Dogs William Becker, * Burton E. Becker, * Mark Handelsman,T Tomas Albrektssons
Twelve 10
Clifford Ochsenbein,* and
placed into immediate extraction sockets in dogs. Six PTFE isolated with membranes and 6 sites served as controls. Standardized implants clinical measurements were taken at test and control sites. At 18 weeks the dogs were anesthetized and flaps were laid for the purpose of obtaining clinical measurements. The average gain of bone around augmented implants was 2.6 mm, while control sites had an average bone gain of 1.0 mm. Ridge width adjacent to augmented sites increased by 1.2 mm and control sites had an increased width of 0.6 mm. Histologie evaluation of test and control specimens showed greater bone formation around augmented implants. Implants augmented with PTFE membranes had clinically significant amounts of bone regeneration when compared with controls. / Periodontol 1991; 62:703-709. mm implants were
were
Key Words: Bone regeneration; Osteogenesis; dental implants.
predictability of dental implants to integrate with the surrounding bone has provided the means to restore function to patients who are totally or partially edentulous.1'2 Recently the principle of guided tissue regeneration (GTR) has been applied to dental implants. Membranes are used to create a space and to protect the blood clot over implants in order to preferentially allow bone to grow into the space. Dahlin et al.3 created dehiscence defects over implants placed into the femur of rabbits. Test sites were protected by polytetrafluorethylene (PTFE) membranes, while control sites were unprotected. The membranes were used to prohibit connective tissue from contacting dehisced implant surfaces. At retrieval test sites had an average gain of 3.8 mm of new bone, while control sites had an average gain of 2.2 mm. Becker et al.4 removed P2, P3, and P4 10 weeks prior to implant placement. Implants were placed into the mandible of dogs. Dehiscence defects were created over the labial surfaces of the implants. Test sites were protected by implant augmentation material, while unprotected sites served as controls. Eighteen weeks after initial surgery the sites The
'University of Southern California, School of Dentistry, Los Angeles, CA; University of Texas, School of Dentistry, Department of Periodontics, Houston, TX; private practice, Tucson, AZ. •University of Texas, School of Dentistry, Department of Periodontics, Houston, TX; private practice, Tucson, AZ. •University of Southern California, School of Dentistry, Los Angeles, CA. 'Private practice, Dallas, TX. "Department of Handicapped Research, Goteborg, Sweden.
measured and the implants and surrounding bone were retrieved for histologie evaluation. At 18 weeks the test sites measured an average of 1.38 mm of coronal bone growth, while the control sites had an average of 0.23 mm of new bone. Histologie evaluation demonstrated osseointegration of test and control specimens. Test sites had more bone regeneration and fewer exposed threads when compared with the control specimens. Zablotsky et al.5 removed mandibular posterior teeth in dogs and allowed 12 weeks for healing prior to implant placement. At implant placement, the sites were prepared and prior to placement, dehiscences were produced in the facial alveolar bone. The implants were then placed. PTFE membranes were used to isolate the dehisced hydroxyapatite-coated and titanium implants in dogs. Half of the implants were protected by membranes and the other half served as unprotected controls. The HA-coated PTFE protected implants had an average of 95.17% bone regeneration, while the grit-blasted titanium test implants had 82.8% bone regeneration. The HA-coated control implants had an average of 55% bone regeneration and the titanium implants had an average of 39% bone fill. There may be advantages to placing implants into extraction sockets and protecting them with membranes. Immediate placement of implants into extraction sockets may protect the ridge from resorbing. If ridge height and width can be preserved, longer implants can be placed, thereby increasing the bone volume contacting the implant. Furthermore, immediate implant placement into extraction sites were
704
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
may shorten the time necessary to complete the restorative phase of treatment. It is the purpose of this study to evaluate bone regeneration around implants placed into immediate extraction sockets and protected by implant augmentation material. An immediately-placed implant is defined as an implant placed at the time of tooth extraction. The study will also evaluate the effect of membrane placement on ridge width. Non-membrane treated implant sites will serve as controls.
MATERIALS AND METHODS Three large hound dogs were used for this study. Three weeks prior to the study the animals were anesthetized with Ace promazine and P3 was removed from each of the dogs. The purpose for removing these teeth was to provide adequate flap access during implant placement. Two weeks prior to initiating this study, the dogs' teeth were scaled and polished. One week prior to the study, the dogs' teeth were brushed with Chlorhexidine. The animals were anesthetized with Ace promazine and maintained with nitrous oxide. For anatomic reasons implants were placed in the mandible. Appropriate infiltration anesthesia was administered and P2 and P4 were removed. Test and control sites were chosen by coin flip. After the first test and control sites were chosen, the sites were alternated for the opposite side of the jaw. Mid-crestal incisions were made from the furcation of PI to the mesial aspect of P5. In order to achieve adequate surgical access, short vertical releasing incisions were made at the anterior and posterior aspects of the flaps. Number 10 round acrylic burs under a constant stream of sterile saline were used to enlarge the occlusal aspect of the extraction socket and to create dehiscence defects on the buccal aspect. The sites were prepared as described by Adell6 and 10 mm standard Branemark implants1 were installed in test and control sites. The implants were placed in such a manner that 2 to 4 threads were exposed on the buccal aspect. If a sufficient number of threads was not exposed, a small chisel was used to remove bone from the buccal implant surface. All implants were immobile at the time of placement. Measurements were made with a standardized Williams probe. Photographic documentation was made at the time the measurements were taken and for all surgical steps. Mid-buccal measurements were made from the top of the implant cylinder to the apex of the dehiscence. The width of the defect at the apical and coronal aspects of the dehiscences was also measured. Implant augmentation material* was adjusted to cover the dehiscence and extended over the adjacent bone by 3 to 5 mm in all directions. The augmentation material is manufactured from expanded PTFE and has an outer partially occlusive weave and an inner relatively occlusive design. A rubber dam punch was used to place a small hole in the material. The implant cover screw secured the material to
'Nobelpharma USA, Chicago, IL. #W.L. Gore and Associates, Flagstaff, AZ.
the implant. The width of the alveolar ridge was measured with a 6.5 cm implant caliper.** Buccal-lingual measurements were taken 1 to 2 mm within the lateral borders of the material and one measurement was taken at the midbuccal implant aspect. The surgical area was rinsed and the flaps were sutured with interrupted 4-0 Dexon sutures. The animals were placed on the antibiotic Tribrissen (30 mg/ kg) orally for 7 days and the surgical areas were inspected weekly. At this time the teeth were polished with Chlorhexidine and saline. The dogs were examined bimonthly. At this examination the surgical areas were evaluated for exposure of cover screws or augmentation material and the teeth were polished with Chlorhexidine. If the material became exposed, it was removed between 14 and 20 days after exposure and the material retrieval incisions were resutured. Eighteen weeks post-implant insertion the animals were anesthetized and the areas of surgery were examined and photographed. Mid-crestal incisions were made and buccal-lingual flaps were reflected exposing the implant sites. Photographs were taken. All implants were immobile. Sites which received membranes had clinically evident increases in ridge width. The membranes were firmly adherent to the underlying bone and had to be separated from the bone by sharp dissection. After membrane removal, mid-buccal measurements were taken from the top of the cylinder to the level of alveolar bone. Three measurements were made of the buccal-lingual alveolar ridge width adjacent to the implants. These measurements were averaged and compared with the initial buccal-lingual measurements. The animals were sacrificed, x-rays were taken, and the specimens were removed from the mandibles. Block specimens were fixed in 4% neutral formalin. The specimens were dehydrated and embedded in methyl methacrylate as described by Donath et al.7 Sections were made through the implants and the surrounding undecalcified bone. After grinding the primary sections to a thickness of 10 to 15 µ , they were stained with 1% toluidine blue in a 1% Borax solution mixed in proportions of 4 to 1 with a 1% pyronin-G solution. The interfacial tissue reactions were studied in a Leitz light microscope connected to a Microvid system and an IBM computer. All histologie analyses were performed in a blind manner and the examiner did not know whether he was observing a test or control specimen. RESULTS During the 18-week healing interval, augmentation material became exposed at 4 test sites, while cover screws became exposed at 2 control sites. The material at the test sites became exposed at 12, 19, 27, and 41 days postsurgery, while control cover screws became exposed at 12 and 14 days. The areas of material exposure were examined for inflammation and infection on a weekly basis. Material which became exposed was arbitrarily removed between 14 and **Ace
Dental, Boston, MA.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
Table 1. Mid-Buccal
(in mm)
Subject No.
Site
(PE) (PE) (TO)* (TO)* (BL)* (BL)* mean
s.d.
R L R L R L
Changes
in Bone
Height for Test and
Controls
Tests Exam Exam Exam 2 1 Difference 1 4.0 0.0 4.0 3.0 5.0 0.0 5.0 4.0 3.5 2.0 1.5 3.0 6.0 3.0 3.0 5.0 1.0 6.0 4.0 3.0 4.0 2.5 1.5 4.0
Control Exam 2 Difference
2.0 4.0
0.0 1.0 1.0 0.0 4.0 0.0
4.4 0.92
3.2 1.17
1.0 1.55
1.8 1.41
2.7 1.60
4.2 1.17
3.0 3.0 2.0 5.0
705
All data rounded to nearest decimal; 6; R right; L left. *Sites where material became exposed and was removed. =
=
=
Figure 2. Augmentation material was secured to the implant with the cover screw.
Figure
1.
days
Implants have been placed into immediate extraction sockets.
after exposure. Due to the small sample size, it was not possible to establish a relationship between early membrane removal and increases in bone height (Table 1). The 2 test sites where the material remained unexposed had complete bone regeneration, while the remaining 4 test sites had slight residual areas of thread exposure. When there was exposure of material or cover screws, the exposure was always along the suture line. At 18 weeks the soft tissues adjacent to the implants were relatively uninflamed and all implants were stable. Clinical changes in bone for augmented and control implants can be seen in Figures 1, 2, 3, 4A, and 4B. Changes in mid-implant bone height can be seen in Table 1. The average initial mid-buccal bone height for material augmented sites was 4.4 mm. At retrieval the mean mid implant bone height was 1.8 mm. The average change in bone level for the material augmented sites was 2.6 mm. For controls, the initial mean mid-buccal bone height was 4.2 mm, while at 18 weeks the mean mid-buccal bone level was 3.2 mm. There was a gain of 1 mm. Changes in alveolar ridge width can be seen in Table 2. The average width of the alveolus adjacent to the augmented implants at insertion was 8.1 mm. At 18 weeks the mean alveolar ridge width was 9.2 mm. There was an in-
21
Figure 3. Exposure of implants 18 weeks after initial surgery. Note minimal bone formation adjacent to control implant. The augmentation has remained in position for the entire healing time.
Figure 4A. The augmentation material has been derlying bone. Note increase in bone width. crease
in
dissected from the
ridge width for all material augmented sites.
un-
For
controls, the mean initial alveolar ridge width was 8.5 mm.
At 18 weeks the average alveolar
ridge width was 8.9 mm.
706
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
All data rounded to nearest decimal; 6; R right; L *Sites where material became exposed and was removed. =
=
=
left.
Histological examinations verified the general clinical findings of more bone being present adjacent to membranetreated implants when compared with controls. A statistical comparison could not be performed, as it was difficult to precisely match peripheral sections with corresponding test and controls. In the central sections, cut in the long axis of the specimens, matching was easier; however, the impact of bone growth in this region was most likely not related to membrane placement. When control and test implants were examined histologically, there was generally more bone adjacent to membrane treated implants (Figs. 5A and 5B). Figure 6 demonstrates a specimen with the augmentation material in place. There is mature bone directly beneath the material. In most test sites there were points of direct bone to implant contact (Fig. 7A), while control specimens usually had a soft tissue layer between the implant and bone (Figs. 7B and 7C). In Figure 8A there is a specimen with a retained portion of the membrane. There is profuse new bone formation, with a continuous thin layer of soft tissue separating the membrane from the underlying bone. Figure 8B demonstrates minimal soft tissue inflammation between the membrane and new bone.
FiS"re 5A- Control specimen. marked by an asterisk
Note absence
of bone over threads.
Area
DISCUSSION This study provides preliminary evidence that implants placed into fresh extraction sockets and augmented with PTFE membranes have a greater amount of bone regeneration when compared with unprotected controls. Similarly, ridge width increased adjacent to sites which were augmented with membranes, while non-augmented sites had clinically insignificant increases in ridge width. It is important to
point
out that ridge width measurements were not taken from standardized points and consequently there is a high probability of measurement error. Recognizing that the sample size and increases in ridge width are small, nonetheless, there was an increase in ridge width at each test site. For controls, there were 2 sites which had an increase in ridge width. The trend for augmented sites to have an increase in ridge width might have been more significantly demonstrated with an increase in sample size. It is interesting to note that the material was prematurely removed due to exposure on 4 out of 6 test sites. Due to the small sample size, it was not possible to establish a relationship between premature material removal and increases in bone height. We are presently evaluating this relationship and will be reporting our results in the future.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
707
Figure 5B. Augmented test site demonstrates almost complete formation of new bone over previously exposed threads. New bone marked with circled asterisk.
Figure IB. (arrows). Figure 6. Test site with membrane still in place (arrows). Note vital bone tissue beneath membrane. Bt
=
bone tissue. Ti
=
titanium.
The clinical evidence of bone regeneration was substantiated to a lesser degree by the histologie data. There were 12 possible specimens which could be examined (6 test, 6 controls). There was a tendency for augmented specimens
Control specimen
demonstrating an interfacial thin white line
compared to control sites. Lack of definitive histologie evidence of significant differences between test and control specimens may be related to processing errors. If the specimens were sectioned tangentially rather than perpendicular to the mid-buccal plane, the area of clinical interest might have been missed. Barzilay et al.8 placed an implant into an extraction socket of to have less thread exposure when
708
Figure 8B. Arrows pointing to soft tissue Asterisk is portion of retained membrane.
7C. Control specimen with and bone (asterisks).
Figure
soft
tissue
interface
between
implant
Figure 8A. New bone formation directly beneath the retained membrane surface (asterisk over membrane). The bone was lamellarized.
monkey. The implant was loaded for 6 months. The implant was removed in block and the implant was in contact with bone 58.2% of the implant length. The purpose of placing augmentation material over implants placed into extraction sites is to provide a space for blood clot retention and organization. By excluding flap a
J Periodontol November 1991
GUIDED TISSUE REGENERATION FOR IMMEDIATE IMPLANTS
lining beneath
the membrane.
epithelium and connective tissue, bone can preferentially be allowed to fill the membrane protected space. When placing implants into extraction sites it is important to prevent fibrous tissue from growing between the implant and the adjacent bone defect. If fibrous tissue grows into the defect the possibility for bone ingrowth will be diminished. Histologie examination of membrane-augmented implants demonstrated active bone formation immediately beneath the membrane. Other specimens demonstrated greater bone contact with augmented implants when compared with controls, and generally there was greater bone adjacent to membrane augmented implants. Lazzara9 placed PTFE membranes over implants which were placed into extraction sockets. The membranes were removed between 4 and 6 weeks after surgery. At the second stage procedure there appeared to be varying amounts of bone around the membrane protected implants. Nyman et al.10 reported 2 cases where membranes were used for implants. One implant was placed into an extraction socket and protected by a PTFE membrane. The membrane was removed at the second stage procedure and clinical and radiographie evidence of bone formation was evident around the augmented implant. Becker et al.11 recently reported a surgical technique for attaining flap closure for implants placed into extraction sockets and augmented with PTFE membranes. At the second stage, there was clinical evidence of bone formation around the augmented implants. Clinical trials are currently being performed for the purpose of evaluating the use of augmentation material over implants placed into extraction sockets. CONCLUSION The present study presents evidence that the principles of guided tissue regeneration can be applied to implants placed into fresh extraction sockets which are augmented by membranes. While this study was performed in dogs, there is reasonable evidence to support testing these principles in clinical trials.
Volume 62 Number 11
BECKER, BECKER, HANDELSMAN, OCHSENBEIN, ALBREKTSSON
Acknowledgments
study was supported by W.L. Gore and Associates. Implant equipment was supplied by Nobelpharma, USA.
This
REFERENCES 1. Albrektsson , Dahl E, Enbom L, et al. Osseointegrated oral implants. A Swedish multicenter study of 8139 œnsecutively inserted Nobelpharma implants. / Periodontol 1988; 59:287. 2. van Steenberghe D, Lekholm U, Bolender C, et al. The applicability of osseointegrated implants in the rehabilitation of partial edentulism: A prospective multicenter study on 558 fixtures. IntJ Oral Maxillofac Implants 1990; 5:272. 3. Dahlin C, Sennerby L, Lekholm U, Linde A, Nyman S. Generation of new bone around titanium implants: An experimental study in rabbits. IntJ Oral Maxillofac Implants 1989; 4:19. 4. Becker W, Becker BE, Handlesman M, et al. Bone formation at dehisced dental implant sites treated with implant augmentation material: A pilot study in dogs. Int J Periodontics Restorative Dent 1990; 10:93. 5. Zablotsky M, Meffert R, Caudill R, Evans G. Histological and clinical comparisons of guided tissue regeneration on dehisced HA-coated
6.
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709
and titanium endosseous implant surfaces. A pilot study. Int J Oral Maxilo Implants In press. Adell R, Lekholm U, Branemark P-I. A 15 year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981; 10:87. Donath , Breuner G-A. A method for the study of undecalcified bones and teeth with attached soft tissue. The Saege-Schliff technique. J Oral Pathol 1982; ll:d318. Barzilay I, Graser JGN, Caton J, Shenkle G. Immediate implantation of pure titanium implants into extraction sockets. / Dent Res 1988; 67 (Spec. Issue):234 (Abstr. 234). Lazzara RJ. Immediate implant placement into extraction sites: Surgical and restorative advantages. Int J Periodontics Restorative Dent 1989; 9:333. Nyman S, Lang NP, Buser D, Bragge U. Bone regeneration adjacent to titanium dental implants using guided tissue regeneration: A report of two cases. Int J Oral Maxillofac Implants 1990; 5:9. Becker W, Becker BE. Guided tissue regeneration for implants placed into extraction sockets and for implant dehiscences: Surgical techniques and case reports. Int J Periodontics Restorative Dent 1990; 10:377.
Send
reprint requests to: Dr. William Becker, 801 North Wilmot, Tuc-
son, AZ 85711.
Accepted for publication June 21,
1991.
