IMPLANT DENTISTRY / VOLUME 23, NUMBER 3 2014
289
Evaluation of a Dense Polytetrafluoroethylene Membrane to Increase Keratinized Tissue: A Randomized Controlled Clinical Trial Eliane Porto Barboza, DScD,* Bianca Stutz, MScD,† Denize Mandarino, MScD,‡ Diogo Moreira Rodrigues, MScD,§ and Vinícius Farias Ferreira, MScDk
lveolar bone resorption is a common finding after tooth extraction.1,2 This can make it difficult or even impossible to place dental implants. Therefore, postextraction alveolar ridge preservation is essential to ensure maintenance of ideal vertical and horizontal ridge dimensions and contours required for ideal 3-dimensional implant placement.3 Preservation of soft tissues after tooth extraction is important as well. The presence of an adequate zone of keratinized tissue has been associated with a more stable implant-mucosal barrier.4–7 In addition, a recent study showed that patients presenting thin periodontal phenotype had 4.5 times greater probability to present periimplant disease.8 The techniques of guided bone regeneration have been successfully applied in the treatment of bone defects and for increasing the width and height
A
*Associate Professor, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. †Private Practice, Rio de Janeiro, Brazil. ‡Adjunct Professor, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. §Graduate Student, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. kGraduate Student, Department of Periodontology, State University of Rio de Janeiro, Rio de Janeiro, Brazil.
Reprint requests and correspondence to: Eliane Porto Barboza, DScD, Associate Professor, Fluminense Federal University, Department of Periodontology, Rua Mario Braga 29, Valonguinho, Niterói, Rio de Janeiro 24040-110, Brazil, Phone/Fax: 55 21 2220-6940, E-mail: [email protected] ISSN 1056-6163/14/02303-289 Implant Dentistry Volume 23 Number 3 Copyright © 2014 by Lippincott Williams & Wilkins DOI: 10.1097/ID.0000000000000060
Background: The presence of an adequate zone of keratinized tissue has been associated with implant health. This study evaluated the increasing of the zone of keratinized tissue using dense polytetrafluoroethylene (d-PTFE) membranes over extraction sites, without primary closure. Materials and Methods: Fifteen sites received d-PTFE membranes. The control sites received no membranes. All cases were sutured with no attempt to achieve primary closure. Before surgery, initial measurements of buccal and lingual keratinized tissue were taken from the mucogingival line (MGL) to the most coronal gingival margins. Final measurements were taken from
the buccal MGL to the lingual MGL, 60 and 90 days after extractions. Results: In the test group, a mean increase in the zone of keratinized tissue of 7.06 6 2.63 mm and 6.6 6 2.84 mm was observed in 60 and 90 days, respectively. In the control group, a mean increase of 2.46 6 1.59 mm and 1.40 6 1.40 mm was observed in 60 and 90 days, respectively. Conclusion: Nonexpanded dPTFE membranes can predictably be used to increase the zone of keratinized tissue in preparation to implant placement. (Implant Dent 2014;23:289–294) Key Words: biomaterial, keratinized tissue, guided bone regeneration
of the alveolar ridge in many animal and human studies.9–17 The membrane material with the longest history of use for this purpose is expanded polytetrafluoroethylene (e-PTFE), a nonresorbable synthetic polymer. Despite the high predictability of bone regeneration using e-PTFE barriers, the main disadvantage of this material is that membrane exposure can result in bacterial contamination, inflammation, and subsequent infection, leading to early removal of the membrane. Several investigators have reported a reduced amount of bone fill in these situations.18–20
An alternative to an e-PTFE or resorbable membrane is a dense polytetrafluoroethylene membrane (d-PTFE). In contrast to porous expanded PTFE, d-PTFE has been shown to withstand exposure in the mouth with a low risk of infection.21,22 Consequently, large horizontal flaps and vertical releasing incisions are not necessary to completely cover the membrane in certain clinical situations, such as to provide coverage for particulate grafting materials in relatively intact extraction sites. This is an important advantage of d-PTFE membrane because it may be esthetically
290
EVALUATION
OF A
DENSE PTFE MEMBRANE
advantageous to intentionally leave PTFE exposed to preserve and potentially improve soft tissue architecture.22 The purpose of this study was to clinically evaluate the increase of the zone of keratinized tissue, using d-PTFE membranes without primary closure over mandibular posterior extraction sockets.
MATERIAL
AND
METHODS
This study was performed in compliance with the principles outlined in the Declaration of Helsinki concerning experimentation involving human subjects. Quality assessment was carried out based on the Randomized Controlled Trial (RCT) checklist of the CONSORT statements.23 All procedures and materials in this study were approved through the relevant independent committee on the Ethics of Human Research of Fluminense Federal University (CEP/HUAP #186/05), and the volunteer subjects were informed about the study protocol and required to sign a consent form. Thirty patients participated in this RCT, which took place in the Dental Clinical Research Center at Fluminense Federal University, Rio de Janeiro, Brazil. All patients were in good general health, aged 20 to 60 years, presenting 30 mandibular posterior teeth with indications for extraction because of root fracture, perforation or periapical lesions, and presenting adjacent teeth. Exclusion criteria included debilitating or systemic disease, smokers, allergies, chronic medication, which affect bone metabolism, poor oral hygiene, or any contraindications for surgical treatment. Patients underwent periodontal therapy (when necessary) and were given oral hygiene instruction to reduce the microbial flora and provide an environment conductive to healing. Surgical Procedures
The volunteer subjects were randomly assigned to the tests or control groups using an envelope system distribution provided by the principal investigator. In the test group, 15 extraction sites received d-PTFE membranes. The control group included 15 extraction sites that received no
TO INCREASE
KERATINIZED TISSUE
membranes. The surgical protocol and measurements were the same for both test and control groups. The same surgeon performed all surgeries. Before tooth extractions, initial measurements (t0) were taken in both test and control groups. A customized acrylic template containing vertical grooves, at the mid-facial and mid-lingual, was used as a fixed reference guide to allow reproducible measurements (Fig. 1). From these reference points, the measurements of the buccal and the lingual keratinized tissues were taken from the mucogingival line (MGL) to the most coronal gingival margins, using a periodontal probe (UNC-15; Hu-Friedy Mfg. Inc., Chicago, IL). To evaluate the reliability of this measurement method, before this study, the operator recorded the distance from the MGL to the most coronal gingival margin on 2 different days. These measurements were compared, and the agreement was significant at the level of 0.01. Tooth extractions were performed under local anesthesia. An intrasulcular
BARBOZA
ET AL
Fig. 1. Acrylic template for measurements standardization.
Fig. 2. Test group. Membrane in place. Note that no attempt was made to achieve primary closure.
Fig. 3. A, Membrane aspect right before its removal; B, newly formed tissue immediately after membrane removal.
incision was made extending to the adjacent teeth. No vertical releasing incisions were performed to preserve the MGL in its original position. If necessary, teeth were sectioned within the socket to preserve the bone walls. After the extractions, all sockets were carefully curetted to remove any residual soft tissues. The randomization envelope was opened, and the assigned treatment test (d-PTFE membranedCytoplast Regentex TXT200; Osteogenics Biomedical Inc., Lubbock, TX) or control (no membrane) was revealed to the surgeon.
Fig. 4. Test group 60 days after tooth extraction. Note the preservation of the MGL on its original position and the increase in the zone of keratinized tissue.
IMPLANT DENTISTRY / VOLUME 23, NUMBER 3 2014 The membranes were trimmed and placed over the extraction sockets. In these cases, mini full-thickness flaps (around 3 mm) were performed on buccal and lingual aspects of the teeth to allow membrane placement. In all cases, membranes were intentionally left exposed. Both test and control groups were sutured with no attempt to achieve primary closure (Fig. 2).
MEDICATION AND POSTOPERATIVE CARE Patients were prescribed systemic antibiotic (amoxicillin 500 mg 3 times a day for 7 days after surgery) and analgesics (acetaminophen 750 mgd6/6 hours for 3 days). All patients rinsed twice daily with 0.12% chlorhexidine digluconate solution (Periogard; Colgate-Palmolive, São Paulo, Brazil) until membrane removal. Sutures were removed 7 days after surgery. In the test group, membranes were removed 28 days after surgery. No surgical procedures were necessary during membrane removal. The epithelial tissue formed between flap and membrane was removed using periodontal curettes to make it possible to expose the connective tissue. The
neoformed tissue was not disturbed (Fig. 3, A and B). Sixty and ninety days after tooth extractions, patients were re-evaluated and new measurements were taken (t1 and t2, respectively). Aspects such as color, texture, and presence or absence of signs of inflammation or infection were also observed. In the test and control groups, new measurements were performed similarly, with the aid of a very thin milimetric ruler placed from the buccal MGL to the lingual MGL, using the reference point. The increase in the zone of keratinized tissue was evaluated by comparison of initial and final measurements (t1 − t0 for 60 days and t2 − t0 for 90 days). A statistical analysis was performed with the Mann-Whitney test. A 5% level of significance and a 95% confidence interval were set for all statistical procedures. The statistical software SPSS for Windows (SPSS 13.0; SPSS Inc., Chicago, IL) was used throughout.
RESULTS None of the patients involved in this study reported any unusual pain or discomfort, abscess, swelling, or allergic
291
reactions during the course of treatment. Although plaque accumulation was observed on surfaces of the intentionally exposed membranes, no signs of tissue inflammation or exudate were detected. Soft tissue presenting macroscopic characteristics of normal keratinized gingiva, such as color, consistency, and texture was observed in all cases. Clinically, the original MGL position seemed to be preserved (Fig. 4). The results of this study are shown in Table 1 (test group) and Table 2 (control group). A mean increase of 7.06 6 2.63 mm and 2.46 6 1.59 mm was observed after 60 days (t1) in the test and control groups, respectively (Tables 1 and 2). After 90 days (t2), a mean increase of 6.6 6 2.84 mm and 1.40 6 1.40 mm was observed in the test and control groups, respectively. A decrease was observed in these measurements in both groups between 60 and 90 days (t2 − t1). The test and control group showed a mean decrease of 0.46 6 1.12 mm and the control group 1.06 6 0.59 mm, respectively (Tables 1 and 2). Tissue measurements did not present normal distribution allowing nonparametric test (Shapiro-Wilk P . 0.05). The Mann-Whitney test showed statistically significant differences
Table 1. Test Group Description and Measurements Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Minimum Maximum SD
Gender
Age
Tooth
F M F F F F M M F F F M M M F
45 27 60 40 35 52 48 48 48 47 28 22 35 28 45 40.53 22 60 10.89
30 29 30 19 19 18 30 19 30 29 28 30 31 18 20
t0 (mm)
t1 (mm)
t2 (mm)
t1 − t0 (mm)
t2 − t0 (mm)
t2 − t1 (mm)
8 15 10 5 8 8 10 10 10 8 13 19 17 13 13 11.13 5 19 3.81
14 19 16 7 14 14 17 20 19 14 22 32 26 20 19 18.2 7 32 5.83
12 19 16 7 14 14 13 19 19 14 22 32 26 20 19 17.73 7 32 6.07
6 4 6 2 6 6 7 10 9 6 9 13 9 7 6 7.06 2 13 2.63
4 4 6 2 6 6 3 9 9 6 9 13 9 7 6 6.6 2 13 2.84
−2 0 0 0 0 0 −4 −1 0 0 0 0 0 0 0 −0.46 −4 0 1.12
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction; t1 − t0, increase of the zone of keratinized tissue after 60 days post-extraction; t2 − t0, increase of the zone of keratinized tissue 90 days post-extraction.
292
EVALUATION
OF A
DENSE PTFE MEMBRANE
TO INCREASE
KERATINIZED TISSUE
BARBOZA
ET AL
Table 2. Control Group Description and Measurements Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Minimum Maximum SD
Gender
Age
Tooth
F F F F F M M F F F F F F F F
43 43 43 45 45 45 56 32 20 20 40 40 40 41 40 39.53 20 56 9.33
30 31 18 30 29 31 30 29 19 30 30 31 18 30 29
t0 (mm)
t1 (mm)
t2 (mm)
t1 − t0 (mm)
t2 − t0 (mm)
t2 − t1 (mm)
8 7 9 10 7 8 4 7 10 11 10 10 9 11 8 8.6 4 11 1.88
12 10 12 11 10 10 2 10 11 14 14 14 13 13 10 11.06 2 14 2.96
11 9 11 11 9 8 2 8 10 12 13 13 12 12 9 10 2 13 2.77
4 3 3 1 3 2 −2 3 1 3 4 4 4 2 2 2.46 −2 4 1.59
3 2 2 1 2 0 −2 1 0 1 3 3 3 1 1 1.4 −2 3 1.40
−1 −1 −1 0 −1 −2 0 −2 −1 −2 −1 −1 −1 −1 −1 −1.06 −2 0 0.59
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction; t1 − t0, increase of the zone of keratinized tissue after 60 days post-extraction; t2 − t0, increase of the zone of keratinized tissue 90 days post-extraction.
Table 3. Statistical Analysis Results Shapiro-Wilk
Mann-Whitney
t
Group
n
P
df
Mean Rank
t0
Test Control Test Control Test Control
15 15 15 15 15 15
0.339 0.151 0.347 0.001 0.476 0.011
15 15 15 15 15 15
18.47 12.53 21.67 9.33 21.77 9.23
t1 t2
P 0.60 ,0.05 ,0.05
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction.
between test and control groups (P , 0.05) for t1 and t2. Note that the initial measurement (t0) presented no significant difference between groups (Table 3).
DISCUSSION This clinical study demonstrated that the use of a d-PTFE membrane, without primary closure, allowed a significant increase of the zone of keratinized tissue after tooth extraction. In the last decade, a host of membrane materials including e-PTFE membranes, collagen, and resorbable polymers have been used in guided bone regeneration. Among the disadvantages of e-PTFE, used as a biomaterial in the
oral cavity, is that the highly porous areas of the membrane, if exposed, are vulnerable to heavy bacterial colonization. This bacterial contamination may result in infection and soft-tissue complications,24–26 which may compromise the results of the regeneration procedure or result in a total failure of the procedure. Therefore, to achieve predictable results, e-PTFE membranes are required to remain completely covered by the soft tissues for a period of time sufficient to allow bone regeneration and maturation.27 It is precisely this requirement for primary closure that makes e-PTFE and many resorbable membranes unsuitable for use to cover extraction sites where they may become exposed.21,28
In contrast, the high-density structure of d-PTFE reduces the risk of bacterial penetration through the membrane, thus eliminating the need for primary closure.22 Therefore, the development of large flaps and vertical releasing incisions to achieve primary closure are not required. In this study, clinical observations showed that there were no signs of postoperative wound infection, and the tissue surrounding the intentionally exposed membranes was found to be healthy. In this study, tooth extraction was performed, endeavoring to keep all bone walls intact in both groups. In addition, in the test group, d-PTFE membrane was placed with no biomaterial filling the sockets. The architecture of the existing bony walls was sufficient to maintain the clot and support d-PTFE membrane in place, preventing a possible collapse of the membrane. These results are in agreement with a study29 that also used d-PTFE membranes without graft materials in alveolar sockets exhibiting all bone walls. In the test group, the membrane was removed 28 days after surgery. This protocol was based on a variety of studies21,22,24,29–32 in which membrane
IMPLANT DENTISTRY / VOLUME 23, NUMBER 3 2014 removal occurred between 21 and 28 days. However, the optimum time for membrane removal is still controversial. An animal study33 reported no significant difference in regenerative results when nonresorbable barriers were removed after 1 month and when they were removed after longer periods. Another advantage of d-PTFE membranes is that the high density of this material makes membrane removal easy, avoiding the need for a difficult second surgery. Removal is simplified by the fact that the membrane is already exposed and visible at the surgical site, and no local anesthetic or flap dissection is required. In this study, membranes were easily removed with no injuries to the underlying neoformed tissues or discomfort to patient. In this study, data analysis showed an increase of the zone of keratinized tissue in both groups. However, soft tissue enhancement was higher in the test group, with a mean increase of 7.06 6 2.63 mm, whereas in the control group the mean was 2.46 6 1.59 mm, after 60 days (t1 − t0). The results of this study are in agreement with previous studies that demonstrated the high predictability of using d-PTFE membranes in alveolar ridge maintenance with concomitant increase of the zone of keratinized tissue.22,24,32,34 It is known that techniques used to achieve primary closure over e-PTFE or resorbable membranes contribute to the loss of keratinized tissue. In contrast, the use of d-PTFE membranes without primary closure allows the clinician to preserve or to increase the zone of keratinized tissue over extraction sites.34 This study showed that it is possible to increase the keratinized tissue zone in preparation for implant placement. A recent study8 showed that patients presenting thin periodontal phenotype had 4.5 times greater probability to present periimplant disease. In addition, a lack of keratinized mucosa surrounding an implant was associated with more plaque accumulation, tissue inflammation, mucosal recession, and loss of attachment.35 Nevertheless, ridge maintenance procedure using intentionally exposed d-PTFE membranes leads to keratinized tissue formation, preparing the post-extraction
sites to implant placement, with less risk of periimplant disease.
CONCLUSIONS The use of d-PTFE membranes, intentionally exposed in post-extraction sites, predictably led to an increase of the zone of keratinized tissue. Post-extraction sites with d-PTFE membranes showed higher keratinized tissue formation than sites that did not receive the membrane.
DISCLOSURE The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
ACKNOWLEDGMENTS The authors thank Osteogenics Biomedical for providing the d-PTFE membranes.
REFERENCES 1. Atwood DA. Reduction of residual ridges: A major oral disease entity. J Prosthet Dent. 1971;26:266–279. 2. Pietrokovski J, Massler M. Residual ridge remodeling after tooth extraction in monkeys. J Prosthet Dent. 1971;26: 119–129. 3. Iasella JM, Greenwell H, Miller RL, et al. Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: A clinical and histologic study in humans. J Periodontol. 2003;74: 990–999. 4. Bengazi F, Wennstrom JL, Lekholm U. Recession of the soft tissue margin at oral implants. A 2-year longitudinal prospective study. Clin Oral Implants Res. 1996;7:303–310. 5. Berglundh T, Lindhe J. Dimension of the periimplant mucosa. Biological width revisited. J Clin Periodontol. 1996;23: 971–973. 6. Moon IS, Berglundh T, Abrahamsson I, et al. The barrier between the keratinized mucosa and the dental implant. An experimental study in the dog. J Clin Periodontol. 1999;26:658– 663. 7. Jeong SM, Choi BH, Li J, et al. The effect of thick mucosa on peri-implant tissues: An experimental study in dogs. J Periodontol. 2008;79:2151–2155. 8. Casado PL, Canullo L, Filardy A, et al. Interleukins 1-b and 10 expressions
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in the peri-implant crevicular fluid from patients with untreated peri-implant disease. Implant Dent (Print). 2013;22:143–150. 9. Dahlin C, Linde A, Gottlow J, et al. Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg. 1988; 81:672–676. 10. Dahlin C, Gottlow J, Linde A, et al. Healing of maxillary and mandibular bone defects using a membrane technique. An experimental study in monkeys. Scand J Plast Reconstr Surg Hand Surg. 1990; 24:13–19. 11. Buser D, Bragger U, Lang NP, et al. Regeneration and enlargement of jaw bone using guided tissue regeneration. Clin Oral Implants Res. 1990;1:22–32. 12. Becker W, Becker B. Guided tissue regeneration for implants placed into extraction sockets and for implant dehiscences: Surgical techniques and case reports. Int J Periodont Rest Dent. 1990;10: 377–391. 13. Nyman S. Bone regeneration using the principle of guided tissue regeneration. J Clin Periodontol. 1991;18:494–498. 14. Nevins M, Mellonig JT. Enhancement of the damaged edentulous ridge to receive dental implants: A combination of allograft and the Gore-Tex membrane. Int J Periodont Rest Dent. 1992;12:97– 111. 15. Barboza EP. Regeneration of Surgically Reduced Alveolar Ridges Using Demineralized Freeze-dried Bone Cortical Columns and Membrane in Dogs: A Clinical and Histological Study. Doctor Science Thesis, Boston, MA: Boston University; 1993:155. 16. Lang NP, Hämmerle CH, Brägger U, et al. Guided tissue regeneration in jawbone defects prior to implant placement. Clin Oral Impl Res. 1994;5:92–97. 17. Barboza EP. Clinical and histologic evaluation of the demineralized freezedried bone membrane used for ridge augmentation. Int J Periodontics Restorative Dent. 1999;19:601–607. 18. Barboza EP. Localized ridge maintenance using bone membrane. Implant Dent. 1999;8:167–172. 19. Jovanovic SA, Spiekermann H, Richter EJ. Bone regeneration around titanium dental implants in dehisced defects sites: A clinical study. Int J Oral Maxillofac Implants. 1992;7:233–245. 20. Becker W, Dahlin C, Becker BE, et al. The use of e-PTFE barrier membranes for bone promotion around titanium implants placed into extraction sockets: A prospective multicenter study. Int J Oral Maxillofac Implants. 1994;9: 31–40. 21. Simion M, Baldoni M, Rossi P, et al. A comparative study of the effectiveness of e-PTFE membranes with and with-
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out early exposure during the healing period. Int J Periodontics Restorative Dent. 1994;14:167–180. 22. Bartee BK. Evaluation of new polytetrafluoroethylene guided tissue regeneration membrane in healing extraction sites. Compend Contin Educ Dent. 1998;19: 1256–1258, 1260, 1262–1264. 23. Schulz KF, Altman DG, Moher D. Consort 2010 statement: Updated guidelines for reporting parallel group randomized trials. Obstet Gynecol. 2010;115: 1063–1070. 24. Bartee BK. Extraction site reconstruction for alveolar ridge preservation. Part 2: Membrane assisted surgical technique. J Oral Implantol. 2001;27:194–197. 25. Bartee BK. The use of high-density polytetrafluoroethylene membrane to treat osseous defects: Clinical reports. Implant Dent. 1995;4:21–26. 26. Fiorellini JP, Engebretson SP, Donath K, et al. Guided bone regeneration utilizing expanded polytetrafluoroethylene membranes in combination with submerged and non submerged dental
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KERATINIZED TISSUE
implants in beagle dogs. J Periodontol. 1998;69:528–535. 27. Macdonald ES, Nowzari H, Contreras A, et al. Clinical and microbiological evaluation of bioabsorbable and a nonresorbable barrier membrane in the treatment of periodontal intraosseous lesions. J Periodontol. 1998;69:445–453. 28. Simion M, Scarano A, Gionso L, et al. Guided bone regeneration using resorbable and nonresorbable membranes: A comparative histologic study in humans. Int J Oral Maxillofac Implants. 1996;11:735–742. 29. Barber HD, Lignelli J, Smith BM, et al. Using a dense PTFE membrane without primary closure to achieve bone and tissue regeneration. J Oral Maxillofac Surg. 2007;65:748–752. 30. Bartee BK, Carr JA. Evaluation of a high-density polytetrafluoroethylene (n-PTFE) membrane as a barrier material to facilitate guided bone regeneration in the rat mandible. J Oral Implantol. 1995; 21:88–95. 31. Bartee BK. A membrane and graft technique for ridge maintenance using
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high-density polytetrafluoroethylene membrane (n-PTFE) and hydroxyapatite: Report of four cases. Tex Dent J. 1995; 112:7–16. 32. Hoffmann O, Bartee BK, Beaumont C, et al. Alveolar bone preservation in extraction sockets using non-resorbable d-PTFE membranes: A retrospective nonrandomized study. J Periodontol. 2008;79: 1355–1369. 33. Vergara JA, Quiñones CR, Nasjleti CE, et al. Vascular response to guided tissue regeneration procedures using nonresorbable and bioabsorbable membranes in dogs. J Periodontol. 1997;68: 217–224. 34. Barboza EP, Stutz B, Ferreira VF, et al. Guided bone regeneration using polytetrafluoroethylene membranes in preparation for dental implant placementsdA report of 420 cases. Implant Dent. 2010; 19:2–7. 35. Lin GH, Chan HL, Wang HL. The significance of keratinized mucosa on implant health: A systematic review. J Periodontol. 2013;84:1755–1767.
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Evaluation of a Dense Polytetrafluoroethylene Membrane to Increase Keratinized Tissue: A Randomized Controlled Clinical Trial Eliane Porto Barboza, DScD,* Bianca Stutz, MScD,† Denize Mandarino, MScD,‡ Diogo Moreira Rodrigues, MScD,§ and Vinícius Farias Ferreira, MScDk
lveolar bone resorption is a common finding after tooth extraction.1,2 This can make it difficult or even impossible to place dental implants. Therefore, postextraction alveolar ridge preservation is essential to ensure maintenance of ideal vertical and horizontal ridge dimensions and contours required for ideal 3-dimensional implant placement.3 Preservation of soft tissues after tooth extraction is important as well. The presence of an adequate zone of keratinized tissue has been associated with a more stable implant-mucosal barrier.4–7 In addition, a recent study showed that patients presenting thin periodontal phenotype had 4.5 times greater probability to present periimplant disease.8 The techniques of guided bone regeneration have been successfully applied in the treatment of bone defects and for increasing the width and height
A
*Associate Professor, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. †Private Practice, Rio de Janeiro, Brazil. ‡Adjunct Professor, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. §Graduate Student, Department of Periodontology, Fluminense Federal University, Rio de Janeiro, Brazil. kGraduate Student, Department of Periodontology, State University of Rio de Janeiro, Rio de Janeiro, Brazil.
Reprint requests and correspondence to: Eliane Porto Barboza, DScD, Associate Professor, Fluminense Federal University, Department of Periodontology, Rua Mario Braga 29, Valonguinho, Niterói, Rio de Janeiro 24040-110, Brazil, Phone/Fax: 55 21 2220-6940, E-mail: [email protected] ISSN 1056-6163/14/02303-289 Implant Dentistry Volume 23 Number 3 Copyright © 2014 by Lippincott Williams & Wilkins DOI: 10.1097/ID.0000000000000060
Background: The presence of an adequate zone of keratinized tissue has been associated with implant health. This study evaluated the increasing of the zone of keratinized tissue using dense polytetrafluoroethylene (d-PTFE) membranes over extraction sites, without primary closure. Materials and Methods: Fifteen sites received d-PTFE membranes. The control sites received no membranes. All cases were sutured with no attempt to achieve primary closure. Before surgery, initial measurements of buccal and lingual keratinized tissue were taken from the mucogingival line (MGL) to the most coronal gingival margins. Final measurements were taken from
the buccal MGL to the lingual MGL, 60 and 90 days after extractions. Results: In the test group, a mean increase in the zone of keratinized tissue of 7.06 6 2.63 mm and 6.6 6 2.84 mm was observed in 60 and 90 days, respectively. In the control group, a mean increase of 2.46 6 1.59 mm and 1.40 6 1.40 mm was observed in 60 and 90 days, respectively. Conclusion: Nonexpanded dPTFE membranes can predictably be used to increase the zone of keratinized tissue in preparation to implant placement. (Implant Dent 2014;23:289–294) Key Words: biomaterial, keratinized tissue, guided bone regeneration
of the alveolar ridge in many animal and human studies.9–17 The membrane material with the longest history of use for this purpose is expanded polytetrafluoroethylene (e-PTFE), a nonresorbable synthetic polymer. Despite the high predictability of bone regeneration using e-PTFE barriers, the main disadvantage of this material is that membrane exposure can result in bacterial contamination, inflammation, and subsequent infection, leading to early removal of the membrane. Several investigators have reported a reduced amount of bone fill in these situations.18–20
An alternative to an e-PTFE or resorbable membrane is a dense polytetrafluoroethylene membrane (d-PTFE). In contrast to porous expanded PTFE, d-PTFE has been shown to withstand exposure in the mouth with a low risk of infection.21,22 Consequently, large horizontal flaps and vertical releasing incisions are not necessary to completely cover the membrane in certain clinical situations, such as to provide coverage for particulate grafting materials in relatively intact extraction sites. This is an important advantage of d-PTFE membrane because it may be esthetically
290
EVALUATION
OF A
DENSE PTFE MEMBRANE
advantageous to intentionally leave PTFE exposed to preserve and potentially improve soft tissue architecture.22 The purpose of this study was to clinically evaluate the increase of the zone of keratinized tissue, using d-PTFE membranes without primary closure over mandibular posterior extraction sockets.
MATERIAL
AND
METHODS
This study was performed in compliance with the principles outlined in the Declaration of Helsinki concerning experimentation involving human subjects. Quality assessment was carried out based on the Randomized Controlled Trial (RCT) checklist of the CONSORT statements.23 All procedures and materials in this study were approved through the relevant independent committee on the Ethics of Human Research of Fluminense Federal University (CEP/HUAP #186/05), and the volunteer subjects were informed about the study protocol and required to sign a consent form. Thirty patients participated in this RCT, which took place in the Dental Clinical Research Center at Fluminense Federal University, Rio de Janeiro, Brazil. All patients were in good general health, aged 20 to 60 years, presenting 30 mandibular posterior teeth with indications for extraction because of root fracture, perforation or periapical lesions, and presenting adjacent teeth. Exclusion criteria included debilitating or systemic disease, smokers, allergies, chronic medication, which affect bone metabolism, poor oral hygiene, or any contraindications for surgical treatment. Patients underwent periodontal therapy (when necessary) and were given oral hygiene instruction to reduce the microbial flora and provide an environment conductive to healing. Surgical Procedures
The volunteer subjects were randomly assigned to the tests or control groups using an envelope system distribution provided by the principal investigator. In the test group, 15 extraction sites received d-PTFE membranes. The control group included 15 extraction sites that received no
TO INCREASE
KERATINIZED TISSUE
membranes. The surgical protocol and measurements were the same for both test and control groups. The same surgeon performed all surgeries. Before tooth extractions, initial measurements (t0) were taken in both test and control groups. A customized acrylic template containing vertical grooves, at the mid-facial and mid-lingual, was used as a fixed reference guide to allow reproducible measurements (Fig. 1). From these reference points, the measurements of the buccal and the lingual keratinized tissues were taken from the mucogingival line (MGL) to the most coronal gingival margins, using a periodontal probe (UNC-15; Hu-Friedy Mfg. Inc., Chicago, IL). To evaluate the reliability of this measurement method, before this study, the operator recorded the distance from the MGL to the most coronal gingival margin on 2 different days. These measurements were compared, and the agreement was significant at the level of 0.01. Tooth extractions were performed under local anesthesia. An intrasulcular
BARBOZA
ET AL
Fig. 1. Acrylic template for measurements standardization.
Fig. 2. Test group. Membrane in place. Note that no attempt was made to achieve primary closure.
Fig. 3. A, Membrane aspect right before its removal; B, newly formed tissue immediately after membrane removal.
incision was made extending to the adjacent teeth. No vertical releasing incisions were performed to preserve the MGL in its original position. If necessary, teeth were sectioned within the socket to preserve the bone walls. After the extractions, all sockets were carefully curetted to remove any residual soft tissues. The randomization envelope was opened, and the assigned treatment test (d-PTFE membranedCytoplast Regentex TXT200; Osteogenics Biomedical Inc., Lubbock, TX) or control (no membrane) was revealed to the surgeon.
Fig. 4. Test group 60 days after tooth extraction. Note the preservation of the MGL on its original position and the increase in the zone of keratinized tissue.
IMPLANT DENTISTRY / VOLUME 23, NUMBER 3 2014 The membranes were trimmed and placed over the extraction sockets. In these cases, mini full-thickness flaps (around 3 mm) were performed on buccal and lingual aspects of the teeth to allow membrane placement. In all cases, membranes were intentionally left exposed. Both test and control groups were sutured with no attempt to achieve primary closure (Fig. 2).
MEDICATION AND POSTOPERATIVE CARE Patients were prescribed systemic antibiotic (amoxicillin 500 mg 3 times a day for 7 days after surgery) and analgesics (acetaminophen 750 mgd6/6 hours for 3 days). All patients rinsed twice daily with 0.12% chlorhexidine digluconate solution (Periogard; Colgate-Palmolive, São Paulo, Brazil) until membrane removal. Sutures were removed 7 days after surgery. In the test group, membranes were removed 28 days after surgery. No surgical procedures were necessary during membrane removal. The epithelial tissue formed between flap and membrane was removed using periodontal curettes to make it possible to expose the connective tissue. The
neoformed tissue was not disturbed (Fig. 3, A and B). Sixty and ninety days after tooth extractions, patients were re-evaluated and new measurements were taken (t1 and t2, respectively). Aspects such as color, texture, and presence or absence of signs of inflammation or infection were also observed. In the test and control groups, new measurements were performed similarly, with the aid of a very thin milimetric ruler placed from the buccal MGL to the lingual MGL, using the reference point. The increase in the zone of keratinized tissue was evaluated by comparison of initial and final measurements (t1 − t0 for 60 days and t2 − t0 for 90 days). A statistical analysis was performed with the Mann-Whitney test. A 5% level of significance and a 95% confidence interval were set for all statistical procedures. The statistical software SPSS for Windows (SPSS 13.0; SPSS Inc., Chicago, IL) was used throughout.
RESULTS None of the patients involved in this study reported any unusual pain or discomfort, abscess, swelling, or allergic
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reactions during the course of treatment. Although plaque accumulation was observed on surfaces of the intentionally exposed membranes, no signs of tissue inflammation or exudate were detected. Soft tissue presenting macroscopic characteristics of normal keratinized gingiva, such as color, consistency, and texture was observed in all cases. Clinically, the original MGL position seemed to be preserved (Fig. 4). The results of this study are shown in Table 1 (test group) and Table 2 (control group). A mean increase of 7.06 6 2.63 mm and 2.46 6 1.59 mm was observed after 60 days (t1) in the test and control groups, respectively (Tables 1 and 2). After 90 days (t2), a mean increase of 6.6 6 2.84 mm and 1.40 6 1.40 mm was observed in the test and control groups, respectively. A decrease was observed in these measurements in both groups between 60 and 90 days (t2 − t1). The test and control group showed a mean decrease of 0.46 6 1.12 mm and the control group 1.06 6 0.59 mm, respectively (Tables 1 and 2). Tissue measurements did not present normal distribution allowing nonparametric test (Shapiro-Wilk P . 0.05). The Mann-Whitney test showed statistically significant differences
Table 1. Test Group Description and Measurements Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Minimum Maximum SD
Gender
Age
Tooth
F M F F F F M M F F F M M M F
45 27 60 40 35 52 48 48 48 47 28 22 35 28 45 40.53 22 60 10.89
30 29 30 19 19 18 30 19 30 29 28 30 31 18 20
t0 (mm)
t1 (mm)
t2 (mm)
t1 − t0 (mm)
t2 − t0 (mm)
t2 − t1 (mm)
8 15 10 5 8 8 10 10 10 8 13 19 17 13 13 11.13 5 19 3.81
14 19 16 7 14 14 17 20 19 14 22 32 26 20 19 18.2 7 32 5.83
12 19 16 7 14 14 13 19 19 14 22 32 26 20 19 17.73 7 32 6.07
6 4 6 2 6 6 7 10 9 6 9 13 9 7 6 7.06 2 13 2.63
4 4 6 2 6 6 3 9 9 6 9 13 9 7 6 6.6 2 13 2.84
−2 0 0 0 0 0 −4 −1 0 0 0 0 0 0 0 −0.46 −4 0 1.12
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction; t1 − t0, increase of the zone of keratinized tissue after 60 days post-extraction; t2 − t0, increase of the zone of keratinized tissue 90 days post-extraction.
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Table 2. Control Group Description and Measurements Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Minimum Maximum SD
Gender
Age
Tooth
F F F F F M M F F F F F F F F
43 43 43 45 45 45 56 32 20 20 40 40 40 41 40 39.53 20 56 9.33
30 31 18 30 29 31 30 29 19 30 30 31 18 30 29
t0 (mm)
t1 (mm)
t2 (mm)
t1 − t0 (mm)
t2 − t0 (mm)
t2 − t1 (mm)
8 7 9 10 7 8 4 7 10 11 10 10 9 11 8 8.6 4 11 1.88
12 10 12 11 10 10 2 10 11 14 14 14 13 13 10 11.06 2 14 2.96
11 9 11 11 9 8 2 8 10 12 13 13 12 12 9 10 2 13 2.77
4 3 3 1 3 2 −2 3 1 3 4 4 4 2 2 2.46 −2 4 1.59
3 2 2 1 2 0 −2 1 0 1 3 3 3 1 1 1.4 −2 3 1.40
−1 −1 −1 0 −1 −2 0 −2 −1 −2 −1 −1 −1 −1 −1 −1.06 −2 0 0.59
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction; t1 − t0, increase of the zone of keratinized tissue after 60 days post-extraction; t2 − t0, increase of the zone of keratinized tissue 90 days post-extraction.
Table 3. Statistical Analysis Results Shapiro-Wilk
Mann-Whitney
t
Group
n
P
df
Mean Rank
t0
Test Control Test Control Test Control
15 15 15 15 15 15
0.339 0.151 0.347 0.001 0.476 0.011
15 15 15 15 15 15
18.47 12.53 21.67 9.33 21.77 9.23
t1 t2
P 0.60 ,0.05 ,0.05
t0, initial measurement: sum of the measurements from the most center of gingival margin to MGL of both buccal and lingual keratinized tissue; t1, measurements 60 days after tooth extraction; t2, measurements 90 days after tooth extraction.
between test and control groups (P , 0.05) for t1 and t2. Note that the initial measurement (t0) presented no significant difference between groups (Table 3).
DISCUSSION This clinical study demonstrated that the use of a d-PTFE membrane, without primary closure, allowed a significant increase of the zone of keratinized tissue after tooth extraction. In the last decade, a host of membrane materials including e-PTFE membranes, collagen, and resorbable polymers have been used in guided bone regeneration. Among the disadvantages of e-PTFE, used as a biomaterial in the
oral cavity, is that the highly porous areas of the membrane, if exposed, are vulnerable to heavy bacterial colonization. This bacterial contamination may result in infection and soft-tissue complications,24–26 which may compromise the results of the regeneration procedure or result in a total failure of the procedure. Therefore, to achieve predictable results, e-PTFE membranes are required to remain completely covered by the soft tissues for a period of time sufficient to allow bone regeneration and maturation.27 It is precisely this requirement for primary closure that makes e-PTFE and many resorbable membranes unsuitable for use to cover extraction sites where they may become exposed.21,28
In contrast, the high-density structure of d-PTFE reduces the risk of bacterial penetration through the membrane, thus eliminating the need for primary closure.22 Therefore, the development of large flaps and vertical releasing incisions to achieve primary closure are not required. In this study, clinical observations showed that there were no signs of postoperative wound infection, and the tissue surrounding the intentionally exposed membranes was found to be healthy. In this study, tooth extraction was performed, endeavoring to keep all bone walls intact in both groups. In addition, in the test group, d-PTFE membrane was placed with no biomaterial filling the sockets. The architecture of the existing bony walls was sufficient to maintain the clot and support d-PTFE membrane in place, preventing a possible collapse of the membrane. These results are in agreement with a study29 that also used d-PTFE membranes without graft materials in alveolar sockets exhibiting all bone walls. In the test group, the membrane was removed 28 days after surgery. This protocol was based on a variety of studies21,22,24,29–32 in which membrane
IMPLANT DENTISTRY / VOLUME 23, NUMBER 3 2014 removal occurred between 21 and 28 days. However, the optimum time for membrane removal is still controversial. An animal study33 reported no significant difference in regenerative results when nonresorbable barriers were removed after 1 month and when they were removed after longer periods. Another advantage of d-PTFE membranes is that the high density of this material makes membrane removal easy, avoiding the need for a difficult second surgery. Removal is simplified by the fact that the membrane is already exposed and visible at the surgical site, and no local anesthetic or flap dissection is required. In this study, membranes were easily removed with no injuries to the underlying neoformed tissues or discomfort to patient. In this study, data analysis showed an increase of the zone of keratinized tissue in both groups. However, soft tissue enhancement was higher in the test group, with a mean increase of 7.06 6 2.63 mm, whereas in the control group the mean was 2.46 6 1.59 mm, after 60 days (t1 − t0). The results of this study are in agreement with previous studies that demonstrated the high predictability of using d-PTFE membranes in alveolar ridge maintenance with concomitant increase of the zone of keratinized tissue.22,24,32,34 It is known that techniques used to achieve primary closure over e-PTFE or resorbable membranes contribute to the loss of keratinized tissue. In contrast, the use of d-PTFE membranes without primary closure allows the clinician to preserve or to increase the zone of keratinized tissue over extraction sites.34 This study showed that it is possible to increase the keratinized tissue zone in preparation for implant placement. A recent study8 showed that patients presenting thin periodontal phenotype had 4.5 times greater probability to present periimplant disease. In addition, a lack of keratinized mucosa surrounding an implant was associated with more plaque accumulation, tissue inflammation, mucosal recession, and loss of attachment.35 Nevertheless, ridge maintenance procedure using intentionally exposed d-PTFE membranes leads to keratinized tissue formation, preparing the post-extraction
sites to implant placement, with less risk of periimplant disease.
CONCLUSIONS The use of d-PTFE membranes, intentionally exposed in post-extraction sites, predictably led to an increase of the zone of keratinized tissue. Post-extraction sites with d-PTFE membranes showed higher keratinized tissue formation than sites that did not receive the membrane.
DISCLOSURE The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
ACKNOWLEDGMENTS The authors thank Osteogenics Biomedical for providing the d-PTFE membranes.
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