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Root resorption and ankylosis associated with guided tissue regeneration
C L I N I C A L
P R A C T I C E
CASE REPORT
Root resorption and ankylosis associated with guided tissue regeneration PATRICIA RAMOS CURY, D.D.S., M.S., Ph.D.; CRISTIANE FURUSE, D.D.S., M.S., Ph.D.; MARÍLIA TRIERVEILER MARTINS, D.D.S., Ph.D.; ENILSON A. SALLUM, D.D.S., M.S., Ph.D.; NEY SOARES DE ARAÚJO, D.D.S., M.S., Ph.D.
uided tissue regeneration (GTR), a regenerative surgical technique, has been evaluated in several controlled clinical trials. Favorable clinical results have been reported for treatment of Class II furcation defects in mandibular molars. Cury and colleagues1 and Lekovic and colleagues2 reported significant probing depth reductions, gains in horizontal and vertical clinical attachment levels and bone height gain, as well as the possibility of complete closure of some Class This case II furcation defects after GTR. GTR involves placement of a memreport and brane between the root surface and the other studies mucoperiosteal flap. This may prevent suggest a high the epithelium and the gingival connecrisk of root tive tissue of the flap from contacting resorption and the root surface, allowing the periankylosis after odontal ligament cells to repopulate this guided tissue surface and regenerate cementum, periodontal ligament and alveolar bone.3 regeneration. However, preventing apical migration of the epithelium poses a risk of producing root resorption, which means that cells from bone and gingival connective tissue (which are able to induce root resorption and ankylosis) may repopulate the root surface before periodontal ligament cells do so.4-6 Several authors have reported that root surface resorption and ankylosis were sequelae to periodontal healing after GTR therapy.7-12 GTR has resulted in the development of several types of membranes. After publication of the initial case report
G
ABSTRACT Background. Root resorption and ankylosis have been reported rarely as sequelae to guided tissue regeneration (GTR). The authors describe a clinical case of root resorption following GTR that involved the use of a bioabsorbable membrane. Case Description. Two years after GTR was performed on a Class II furcation defect, the clinical examination revealed root resorption reaching the pulp chamber. The furcation defect was filled with epithelium and connective tissue, which contained inflammatory infiltrate and fragments of the membrane. The authors also observed areas of the tooth that exhibited points of ankylosis and root resorption. Clinical Implications. Clinical trials have reported favorable clinical and histologic results with GTR. However, this case report, along with other case reports and studies in animals, suggests a high risk of root resorption and ankylosis after GTR, which could limit the indications for this technique. Key Words. Periodontal surgery; guided tissue regeneration; bioabsorbable membranes; furcation therapy; root resorption; ankylosis.
involving the use of a millipore filter,13 nonresorbable membranes were used, which must be removed in a second surgical procedure. This shortcoming was resolved by using bioabsorbable barriers. Most bioabsorbable membranes are based on collagen, polylactic acid, polyglycolic acid or copolymers of polylactide-glycolide acid.14 Several authors reported positive results in animals and humans after use of a bioabsorbable polylactic acid membrane (Guidor matrix barrier, Guidor AB, Huddinge, Sweden).1,8,15-18 This product (which is no longer manufactured) was made of amorphous polylactic acid softened with a citric acid ester for malleability, which facilitated clinical handling. Gottlow and colleagues7 and Gottlow16 reported that the matrix barrier
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maintained its functional stability for a minimum of six weeks, after which the membrane was resorbed slowly by hydrolysis, without interfering with the regenerative healing process. Bioresorption of this material was completed within 12 months.7,16 Biomodification of the root surfaces using tetracycline promotes connective tissue attachment in vitro.19 Tetracycline has been used in root coverage procedures,20 flap surgery21 and bone grafting.22 Wikesjö and colleages23 reported the development of root resorption after tetracycline root conditioning in animals, and Ben-Yehouda24 reported it in a patient. We describe a case of root resorption and ankylosis in a tooth that underwent GTR therapy with a bioabsorbable membrane. In addition, a 10 percent tetracycline solution had been applied to the root surface. CASE REPORT
Clinical and radiographic data. In March 1997, a general dentist referred a 40-year-old woman to the Graduate Clinic of the School of Dentistry of Piracicaba, University of Campinas, Brazil, for periodontal treatment. Two of us (P.C., E.S.) diagnosed the patient as having generalized advanced chronic periodontitis, with a Class II furcation defect on the buccal aspect of tooth no. 32. The tooth was vital and had 2 millimeters of keratinized mucosa and 4.4 mm of probing depth. One of us (P.C.) performed the clinical measurements using a University of North Carolina periodontal probe and verified them with a caliper.1 The plaque and gingival index values were 0 (plaque absent) and 2 (bleeding on periodontal probing), respectively.25,26 The patient was a nonsmoker, free of systemic disease and not taking any medications. The clinician performed full-mouth scaling and root planing, removed plaque-retentive factors (such as restorative overhangs) and gave detailed oral hygiene instructions to the patient. She then decided to use GTR to treat the Class II furcation defect. The clinician obtained vertical bitewing radiographs and made probing depth measurements before surgery and at six, 12 and 18 months after surgery. The surgery consisted of making an intrasulcular incision and a mucoperiosteal flap and removing granulation tissue. The clinician carefully removed the epithelium from the inner surface of 338
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the flap. Using manual and rotary instruments, she thoroughly scaled and planed the root surface. She rinsed the area with sterile saline and applied a 10 percent tetracycline solution to the root surface for three minutes. The membrane (Guidor matrix barrier) was fitted to cover the furcation and 3 to 4 mm of alveolar bone beyond the defect. Using the preplaced resorbable ligature, the clinician tightly fit the coronal portion of the membrane to the tooth. She positioned the mucoperiosteal flap coronally and secured it with interdental expanded polytetrafluoroethylene sutures to ensure coverage of the membrane. After surgery, the patient received 100 milligrams of doxycycline per day for two weeks and 0.12 percent chlorhexidine mouthwash twice a day for eight weeks. The dentist removed the flap sutures after 14 days. She saw the patient every two weeks for six months for professional prophylaxis and to reinforce oral hygiene procedures. Thereafter, the dentist saw the patient every three months for 18 months for maintenance therapy. Healing was uneventful in the site, and the membrane did not become exposed. At the one-year follow-up examination, the patient experienced a gain in vertical (2.9 mm) and horizontal (0.3 mm) clinical attachment levels. She also experienced an increase in the gingival recession level (0.8 mm) and a reduction in probing depth (from 4.4 mm to 2.3 mm). Nevertheless, the furcation defect remained classified as a Class II furcation defect. The final plaque and gingival index values were 0 and 1, respectively. No clinical or radiographic complications were present during the first 21 months of followup. Two years after surgery, the patient complained of pain in the tooth. The clinical examination revealed root resorption through the pulpal floor of tooth no. 32. The resorption cavity reached the pulpal chamber. Because the resorption cavity was small, radiographic examination did not reveal the resorption. After surgical inspection, the clinician extracted the tooth. Histologic findings. After extracting the tooth, the clinician immersed it immediately in 10 percent buffered formalin along with the soft tissue filling the furcation defect. After 48 hours, the tooth was decalcified in a solution of 50 percent formic acid and 20 percent sodium citrate at room temperature.
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Figure 1. The furcation defect in the tooth was filled with a hyperplastic epithelium and connective tissue. The connective tissue contained inflammatory infiltrate, which was composed of mononuclear cells and fragments suggestive of the bioabsorbable membrane (arrow) (original magnification × 100, hematoxylin-eosin stain).
After three months, the tooth and soft tissue were washed in running water, dehydrated and embedded in paraffin. The clinician cut serial sections (5 micrometers thick) and stained them with hematoxylin-eosin. We then used light microscopy to examine the sections. RESULTS
The soft tissue that filled the furcation defect was composed of sulcular epithelium overlaying connective tissue that contained inflammatory infiltrate. The inflammatory infiltrate consisted of mononuclear cells and the remainder of the membrane (Figure 1). Figure 2 shows an overview of the mesiodistal section of the tooth. The root surface of the healed furcation defect exhibited areas of ankylosis (Figure 3). We could not see the periodontal ligament in the furcation area, and points of newly formed cementum were thick. We detected several pearls of cementum in the periodontal ligament apical to the furcation area and around the root surface where the membrane had been placed. In addition, we observed resorption cavities in some areas next to the furcation area (Figure 4); however, we did not see any multinucleated cells. DISCUSSION
Although adverse effects are possible after GTR treatment, root resorption7-9 and ankylosis10-12
Figure 2. Overview of the mesiodistal section (boxed-in area) of tooth no. 32 (hematoxylin-eosin stain).
have been reported rarely. In this case, root resorption and ankylosis developed as a late complication of GTR. It is possible that root resorption and ankylosis were induced by the GTR procedure itself, the administration of tetracycline or a combination of the GTR procedure and the tetracycline. Melcher27 postulated that the primary source of cells that repopulate the root surface will determine the healing results. GTR interferes with the normal sequence of events in which undifferentiated ectomesenchymal cells are more likely to migrate into the periodontal defect and root surface,28 where they are able to differentiate into periodontal fibroblasts, cementoblasts or osteoblasts and regenerate periodontal ligament, cementum and alveolar bone, respectively.29 The migration rate of periodontal ligament cells is at least as high as that of bone cells29; thus, it is the ligament cells that first repopulate the root surface. Experiments on the role of various types of tissues involved in periodontal healing have shown
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Figure 3. High-magnification view of a portion of the boxed area in Figure 2 showing ankylosis. Points of newly formed cellular cementum (C) in contact with bone (B) and ankylosis (arrow) were detected. D: Dentin (original magnification × 400, hematoxylin-eosin stain).
Figure 4. High-magnification view of a portion of the boxed area in Figure 2 showing root resorption. The arrow indicates the resorption cavity. C: Cementum. D: Dentin (original magnification × 400, hematoxylin-eosin stain).
that the granulation tissue, derived from bone and gingival connective tissue, induced root resorption rather than the formation of a new connective tissue attachment when growing on the root surface deprived of its periodontal ligament tissue.4-6,29 In our patient, the membrane probably prevented the cells derived from gingival connective tissue from proliferating into the root surface. Thus, it is possible that cells from the nearby bone tissue arrived at the root surface first, induced root resorption and formed bone directly on the dental hard tissue. Furthermore, Blomlöf and Lindskog9 reported that numerous CD68+ cells—both mononuclear and multinucleated—covered resorption cavities; consequently, it also is possible that cells that resorbed the root surface may have been derived from macrophage lineage blood. Despite results showing that bioresorption of this membrane is completed within 12 months,7,16 we found residual membrane in our patient at two years, and it may have had a stimulant or
irritant effect on inflammatory clast cells. In this case, we applied a 10 percent tetracycline solution to the root surface for three minutes before fitting the membrane. The use of tetracycline has gained some interest among clinicians owing to its collagenase-inhibiting potential and acidic and antimicrobial properties.30 Several studies have examined the potential of tetracycline conditioning on root surfaces to promote the formation of new connective tissue attachment. Claffey and colleagues31 reported a gain in connective tissue after the topical use of tetracycline. However, complications such as root resorption and ankylosis also have been observed after application of a tetracycline solution.23,24 Wikesjö and colleagues23 examined the effects of root surface demineralization after tetracycline hydrochloride was applied as an adjunct to reconstructive periodontal surgery. Their study showed that root resorption and ankylosis were prevalent features of the healing process. Furthermore, Ben-Yehouda24 reported a case of progressive cer-
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vical root resorption in a patient who had undergone tetracycline root conditioning and GTR. The author suggested that demineralization of the root surface prevented the colonization of both epithelial and periodontal ligament cells. CONCLUSION
Based on the literature and the findings in the case described above, we believe that the root resorption and ankylosis observed in our patient may have been linked to either the GTR technique or use of tetracycline. Because root surface demineralization with tetracycline hydrochloride does not enhance the results achieved with GTR alone,32 clinicians should avoid its use when performing GTR. ■ Dr. Cury is a postdoctoral researcher, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil, and a professor, Department of Microbiology, São Leopoldo-Mandic Dental Research Institute, R. Abolição, 1827, Campinas, SP, CEP: 13045-610, Brazil, e-mail “[email protected]”. Address reprint requests to Dr. Cury. Dr. Furuse is a professor, Department of Oral Pathology, São Leopoldo-Mandic Dental Research Institute, Campinas, Brazil. Dr. Martins is an assistant professor, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil. Dr. Sallum is an associate professor, Department of Prosthodontics and Periodontics, University of Campinas, School of Dentistry, Brazil. Dr. de Araújo is chairman and a professor, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil. 1. Cury PR, Sallum EA, Nociti FH Jr, Sallum AW, Jeffcoat MK. Long-term results of guided tissue regeneration therapy in the treatment of Class II furcation defects: a randomized clinical trial. J Periodontol 2003;74(1):3-9. 2. Lekovic V, Kenney EB, Kovacevic K, Carranza FA. Evaluation of guided tissue regeneration in Class II furcation defects: a clinical re-entry study. J Periodontol 1989;60:694-8. 3. Caton JG, DeFuria EL, Polson AM, Nyman S. Periodontal regeneration via selective cell repopulation. J Periodontol 1987;58:546-52. 4. Karring T, Nyman S, Lindhe J. Healing following implantation of periodontitis affected roots into bone tissue. J Clin Periodontol 1980;7(2):96-105. 5. Karring T, Nyman S, Lindhe J, Sirirat M. Potentials for root resorption during periodontal wound healing. J Clin Periodontol 1984;11(1):41-52. 6. Nyman S, Karring T, Lindhe J, Planten S. Healing following implantation of periodontitis-affected roots into gingival connective tissue. J Clin Periodontol 1980;7:394-401. 7. Gottlow J, Laurell L, Lundgren D, et al. Periodontal tissue response to a new bioresorbable guided tissue regeneration device: a longitudinal study in monkeys. Int J Periodontics Restorative Dent 1994;14:436-49. 8. Sallum EA, Sallum AW, Nociti FH Jr, Marcantonio RA, de Toledo S. New attachment achieved by guided tissue regeneration using a bioresorbable polylactic acid membrane in dogs. Int J Periodontics Restorative Dent 1998;18:502-10. 9. Blomlöf L, Lindskog S. Cervical root resorption associated with
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guided tissue regeneration: a case report. J Periodontol 1998;69:392-5. 10. Melcher AH. Repair of wounds in the periodontium of the rat: influence of periodontal ligament on osteogenesis. Arch Oral Biol 1970;15:1183-204. 11. Aukhil I, Pettersson E, Suggs C. Guided tissue regeneration: an experimental procedure in beagle dogs. J Periodontol 1986;57:727-34. 12. Caton JG, DeFuria EL, Polson AM, Nyman S. Periodontal regeneration via selective cell repopulation. J Periodontol 1987;58:546-52. 13. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 1982;9:290-6. 14. Gottlow J, Nyman S. Barrier membranes in the treatment of periodontal defects. Curr Opin Periodontol 1996;3:140-8. 15. Araújo MG, Berglundh T, Lindhe J. GTR treatment of degree III furcation defects with 2 different resorbable barriers: an experimental study in dogs. J Clin Periodontol 1998;25:253-9. 16. Gottlow J. Guided tissue regeneration using bioresorbable and non-resorbable devices: initial healing and long-term results. J Periodontol 1993;64(11 supplement):1157-65. 17. Hugoson A, Ravald N, Fornell J, Johard G, Teiwik A, Gottlow J. Treatment of Class II furcation involvements in humans with bioresorbable and nonresorbable guided tissue regeneration barriers: a randomized multi-center study. J Periodontol 1995;66:624-34. 18. De Leonardis D, Garg AK, Pedrazzoli V, Pecora GE. Clinical evaluation of the treatment of Class II furcation involvements with bioabsorbable barriers alone or associated with demineralized freezedried bone allografts. J Periodontol 1999;70(1):8-12. 19. Terranova VP, Franzetti LC, Hic S, et al. A biochemical approach to periodontal regeneration: tetracycline treatment of dentin promotes fibroblast adhesion and growth. J Periodontal Res 1986;21:330-7. 20. Harris RJ. The connective tissue with partial thickness double pedicle graft: the results of 100 consecutively-treated defects. J Periodontol 1994;65:448-61. 21. Alger FA, Solt CW, Vuddhakanok S, Miles K. The histologic evaluation of new attachment in periodontally diseased human roots treated with tetracycline-hydrochloride and fibronectin. J Periodontol 1990;61:447-55. 22. Drury GI, Yukna RA. Histologic evaluation of combining tetracycline and allogeneic freeze-dried bone on bone regeneration in experimental defects in baboons. J Periodontol 1991;62:652-8. 23. Wikesjö UM, Claffey N, Christersson LA, et al. Repair of periodontal furcation defects in beagle dogs following reconstructive surgery including root surface demineralization with tetracycline hydrochloride and topical fibronectin application. J Clin Periodontol 1988;15(1):73-80. 24. Ben-Yehouda A. Progressive cervical root resorption related to tetracycline root conditioning. J Periodontol 1997;68:432-5. 25. Silness JL, Löe H. Periodontal disease in pregnancy, II: correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22:121-35. 26. Löe H, Silness J. Periodontal disease in pregnancy, I: prevalence and severity. Acta Odontol Scand 1963;21:533-51. 27. Melcher AH. On the repair potential of periodontal tissues. J Periodontol 1976;47:256-60. 28. McCulloch CA, Barghava U, Melcher AH. Cell death and the regulation of populations of cells in the periodontal ligament. Cell Tissue Res 1989;255(1):129-38. 29. Nyman S, Gottlow J, Karring T, Lindhe J. The regenerative potential of the periodontal ligament: an experimental study in the monkey. J Clin Periodontol 1982;9:257-65. 30. Wikesjo UM, Baker PJ, Christersson LA, et al. A biochemical approach to periodontal regeneration: tetracycline treatment conditions dentin surfaces. J Periodontal Res 1986;21:322-9. 31. Claffey N, Bogle G, Bjorvatn K, Selvig KA, Egelberg J. Topical application of tetracycline in regenerative periodontal surgery in beagles. Acta Odontol Scand 1987;45(3):141-6. 32. Dyer BL, Caffesse RG, Nasjleti CE, Morrison EC. Guided tissue regeneration with dentin biomodification. J Periodontal 1993;64: 1052-60.
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CASE REPORT
Root resorption and ankylosis associated with guided tissue regeneration PATRICIA RAMOS CURY, D.D.S., M.S., Ph.D.; CRISTIANE FURUSE, D.D.S., M.S., Ph.D.; MARÍLIA TRIERVEILER MARTINS, D.D.S., Ph.D.; ENILSON A. SALLUM, D.D.S., M.S., Ph.D.; NEY SOARES DE ARAÚJO, D.D.S., M.S., Ph.D.
uided tissue regeneration (GTR), a regenerative surgical technique, has been evaluated in several controlled clinical trials. Favorable clinical results have been reported for treatment of Class II furcation defects in mandibular molars. Cury and colleagues1 and Lekovic and colleagues2 reported significant probing depth reductions, gains in horizontal and vertical clinical attachment levels and bone height gain, as well as the possibility of complete closure of some Class This case II furcation defects after GTR. GTR involves placement of a memreport and brane between the root surface and the other studies mucoperiosteal flap. This may prevent suggest a high the epithelium and the gingival connecrisk of root tive tissue of the flap from contacting resorption and the root surface, allowing the periankylosis after odontal ligament cells to repopulate this guided tissue surface and regenerate cementum, periodontal ligament and alveolar bone.3 regeneration. However, preventing apical migration of the epithelium poses a risk of producing root resorption, which means that cells from bone and gingival connective tissue (which are able to induce root resorption and ankylosis) may repopulate the root surface before periodontal ligament cells do so.4-6 Several authors have reported that root surface resorption and ankylosis were sequelae to periodontal healing after GTR therapy.7-12 GTR has resulted in the development of several types of membranes. After publication of the initial case report
G
ABSTRACT Background. Root resorption and ankylosis have been reported rarely as sequelae to guided tissue regeneration (GTR). The authors describe a clinical case of root resorption following GTR that involved the use of a bioabsorbable membrane. Case Description. Two years after GTR was performed on a Class II furcation defect, the clinical examination revealed root resorption reaching the pulp chamber. The furcation defect was filled with epithelium and connective tissue, which contained inflammatory infiltrate and fragments of the membrane. The authors also observed areas of the tooth that exhibited points of ankylosis and root resorption. Clinical Implications. Clinical trials have reported favorable clinical and histologic results with GTR. However, this case report, along with other case reports and studies in animals, suggests a high risk of root resorption and ankylosis after GTR, which could limit the indications for this technique. Key Words. Periodontal surgery; guided tissue regeneration; bioabsorbable membranes; furcation therapy; root resorption; ankylosis.
involving the use of a millipore filter,13 nonresorbable membranes were used, which must be removed in a second surgical procedure. This shortcoming was resolved by using bioabsorbable barriers. Most bioabsorbable membranes are based on collagen, polylactic acid, polyglycolic acid or copolymers of polylactide-glycolide acid.14 Several authors reported positive results in animals and humans after use of a bioabsorbable polylactic acid membrane (Guidor matrix barrier, Guidor AB, Huddinge, Sweden).1,8,15-18 This product (which is no longer manufactured) was made of amorphous polylactic acid softened with a citric acid ester for malleability, which facilitated clinical handling. Gottlow and colleagues7 and Gottlow16 reported that the matrix barrier
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maintained its functional stability for a minimum of six weeks, after which the membrane was resorbed slowly by hydrolysis, without interfering with the regenerative healing process. Bioresorption of this material was completed within 12 months.7,16 Biomodification of the root surfaces using tetracycline promotes connective tissue attachment in vitro.19 Tetracycline has been used in root coverage procedures,20 flap surgery21 and bone grafting.22 Wikesjö and colleages23 reported the development of root resorption after tetracycline root conditioning in animals, and Ben-Yehouda24 reported it in a patient. We describe a case of root resorption and ankylosis in a tooth that underwent GTR therapy with a bioabsorbable membrane. In addition, a 10 percent tetracycline solution had been applied to the root surface. CASE REPORT
Clinical and radiographic data. In March 1997, a general dentist referred a 40-year-old woman to the Graduate Clinic of the School of Dentistry of Piracicaba, University of Campinas, Brazil, for periodontal treatment. Two of us (P.C., E.S.) diagnosed the patient as having generalized advanced chronic periodontitis, with a Class II furcation defect on the buccal aspect of tooth no. 32. The tooth was vital and had 2 millimeters of keratinized mucosa and 4.4 mm of probing depth. One of us (P.C.) performed the clinical measurements using a University of North Carolina periodontal probe and verified them with a caliper.1 The plaque and gingival index values were 0 (plaque absent) and 2 (bleeding on periodontal probing), respectively.25,26 The patient was a nonsmoker, free of systemic disease and not taking any medications. The clinician performed full-mouth scaling and root planing, removed plaque-retentive factors (such as restorative overhangs) and gave detailed oral hygiene instructions to the patient. She then decided to use GTR to treat the Class II furcation defect. The clinician obtained vertical bitewing radiographs and made probing depth measurements before surgery and at six, 12 and 18 months after surgery. The surgery consisted of making an intrasulcular incision and a mucoperiosteal flap and removing granulation tissue. The clinician carefully removed the epithelium from the inner surface of 338
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the flap. Using manual and rotary instruments, she thoroughly scaled and planed the root surface. She rinsed the area with sterile saline and applied a 10 percent tetracycline solution to the root surface for three minutes. The membrane (Guidor matrix barrier) was fitted to cover the furcation and 3 to 4 mm of alveolar bone beyond the defect. Using the preplaced resorbable ligature, the clinician tightly fit the coronal portion of the membrane to the tooth. She positioned the mucoperiosteal flap coronally and secured it with interdental expanded polytetrafluoroethylene sutures to ensure coverage of the membrane. After surgery, the patient received 100 milligrams of doxycycline per day for two weeks and 0.12 percent chlorhexidine mouthwash twice a day for eight weeks. The dentist removed the flap sutures after 14 days. She saw the patient every two weeks for six months for professional prophylaxis and to reinforce oral hygiene procedures. Thereafter, the dentist saw the patient every three months for 18 months for maintenance therapy. Healing was uneventful in the site, and the membrane did not become exposed. At the one-year follow-up examination, the patient experienced a gain in vertical (2.9 mm) and horizontal (0.3 mm) clinical attachment levels. She also experienced an increase in the gingival recession level (0.8 mm) and a reduction in probing depth (from 4.4 mm to 2.3 mm). Nevertheless, the furcation defect remained classified as a Class II furcation defect. The final plaque and gingival index values were 0 and 1, respectively. No clinical or radiographic complications were present during the first 21 months of followup. Two years after surgery, the patient complained of pain in the tooth. The clinical examination revealed root resorption through the pulpal floor of tooth no. 32. The resorption cavity reached the pulpal chamber. Because the resorption cavity was small, radiographic examination did not reveal the resorption. After surgical inspection, the clinician extracted the tooth. Histologic findings. After extracting the tooth, the clinician immersed it immediately in 10 percent buffered formalin along with the soft tissue filling the furcation defect. After 48 hours, the tooth was decalcified in a solution of 50 percent formic acid and 20 percent sodium citrate at room temperature.
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Figure 1. The furcation defect in the tooth was filled with a hyperplastic epithelium and connective tissue. The connective tissue contained inflammatory infiltrate, which was composed of mononuclear cells and fragments suggestive of the bioabsorbable membrane (arrow) (original magnification × 100, hematoxylin-eosin stain).
After three months, the tooth and soft tissue were washed in running water, dehydrated and embedded in paraffin. The clinician cut serial sections (5 micrometers thick) and stained them with hematoxylin-eosin. We then used light microscopy to examine the sections. RESULTS
The soft tissue that filled the furcation defect was composed of sulcular epithelium overlaying connective tissue that contained inflammatory infiltrate. The inflammatory infiltrate consisted of mononuclear cells and the remainder of the membrane (Figure 1). Figure 2 shows an overview of the mesiodistal section of the tooth. The root surface of the healed furcation defect exhibited areas of ankylosis (Figure 3). We could not see the periodontal ligament in the furcation area, and points of newly formed cementum were thick. We detected several pearls of cementum in the periodontal ligament apical to the furcation area and around the root surface where the membrane had been placed. In addition, we observed resorption cavities in some areas next to the furcation area (Figure 4); however, we did not see any multinucleated cells. DISCUSSION
Although adverse effects are possible after GTR treatment, root resorption7-9 and ankylosis10-12
Figure 2. Overview of the mesiodistal section (boxed-in area) of tooth no. 32 (hematoxylin-eosin stain).
have been reported rarely. In this case, root resorption and ankylosis developed as a late complication of GTR. It is possible that root resorption and ankylosis were induced by the GTR procedure itself, the administration of tetracycline or a combination of the GTR procedure and the tetracycline. Melcher27 postulated that the primary source of cells that repopulate the root surface will determine the healing results. GTR interferes with the normal sequence of events in which undifferentiated ectomesenchymal cells are more likely to migrate into the periodontal defect and root surface,28 where they are able to differentiate into periodontal fibroblasts, cementoblasts or osteoblasts and regenerate periodontal ligament, cementum and alveolar bone, respectively.29 The migration rate of periodontal ligament cells is at least as high as that of bone cells29; thus, it is the ligament cells that first repopulate the root surface. Experiments on the role of various types of tissues involved in periodontal healing have shown
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Figure 3. High-magnification view of a portion of the boxed area in Figure 2 showing ankylosis. Points of newly formed cellular cementum (C) in contact with bone (B) and ankylosis (arrow) were detected. D: Dentin (original magnification × 400, hematoxylin-eosin stain).
Figure 4. High-magnification view of a portion of the boxed area in Figure 2 showing root resorption. The arrow indicates the resorption cavity. C: Cementum. D: Dentin (original magnification × 400, hematoxylin-eosin stain).
that the granulation tissue, derived from bone and gingival connective tissue, induced root resorption rather than the formation of a new connective tissue attachment when growing on the root surface deprived of its periodontal ligament tissue.4-6,29 In our patient, the membrane probably prevented the cells derived from gingival connective tissue from proliferating into the root surface. Thus, it is possible that cells from the nearby bone tissue arrived at the root surface first, induced root resorption and formed bone directly on the dental hard tissue. Furthermore, Blomlöf and Lindskog9 reported that numerous CD68+ cells—both mononuclear and multinucleated—covered resorption cavities; consequently, it also is possible that cells that resorbed the root surface may have been derived from macrophage lineage blood. Despite results showing that bioresorption of this membrane is completed within 12 months,7,16 we found residual membrane in our patient at two years, and it may have had a stimulant or
irritant effect on inflammatory clast cells. In this case, we applied a 10 percent tetracycline solution to the root surface for three minutes before fitting the membrane. The use of tetracycline has gained some interest among clinicians owing to its collagenase-inhibiting potential and acidic and antimicrobial properties.30 Several studies have examined the potential of tetracycline conditioning on root surfaces to promote the formation of new connective tissue attachment. Claffey and colleagues31 reported a gain in connective tissue after the topical use of tetracycline. However, complications such as root resorption and ankylosis also have been observed after application of a tetracycline solution.23,24 Wikesjö and colleagues23 examined the effects of root surface demineralization after tetracycline hydrochloride was applied as an adjunct to reconstructive periodontal surgery. Their study showed that root resorption and ankylosis were prevalent features of the healing process. Furthermore, Ben-Yehouda24 reported a case of progressive cer-
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vical root resorption in a patient who had undergone tetracycline root conditioning and GTR. The author suggested that demineralization of the root surface prevented the colonization of both epithelial and periodontal ligament cells. CONCLUSION
Based on the literature and the findings in the case described above, we believe that the root resorption and ankylosis observed in our patient may have been linked to either the GTR technique or use of tetracycline. Because root surface demineralization with tetracycline hydrochloride does not enhance the results achieved with GTR alone,32 clinicians should avoid its use when performing GTR. ■ Dr. Cury is a postdoctoral researcher, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil, and a professor, Department of Microbiology, São Leopoldo-Mandic Dental Research Institute, R. Abolição, 1827, Campinas, SP, CEP: 13045-610, Brazil, e-mail “[email protected]”. Address reprint requests to Dr. Cury. Dr. Furuse is a professor, Department of Oral Pathology, São Leopoldo-Mandic Dental Research Institute, Campinas, Brazil. Dr. Martins is an assistant professor, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil. Dr. Sallum is an associate professor, Department of Prosthodontics and Periodontics, University of Campinas, School of Dentistry, Brazil. Dr. de Araújo is chairman and a professor, Department of Oral Pathology, University of São Paulo, School of Dentistry, Brazil. 1. Cury PR, Sallum EA, Nociti FH Jr, Sallum AW, Jeffcoat MK. Long-term results of guided tissue regeneration therapy in the treatment of Class II furcation defects: a randomized clinical trial. J Periodontol 2003;74(1):3-9. 2. Lekovic V, Kenney EB, Kovacevic K, Carranza FA. Evaluation of guided tissue regeneration in Class II furcation defects: a clinical re-entry study. J Periodontol 1989;60:694-8. 3. Caton JG, DeFuria EL, Polson AM, Nyman S. Periodontal regeneration via selective cell repopulation. J Periodontol 1987;58:546-52. 4. Karring T, Nyman S, Lindhe J. Healing following implantation of periodontitis affected roots into bone tissue. J Clin Periodontol 1980;7(2):96-105. 5. Karring T, Nyman S, Lindhe J, Sirirat M. Potentials for root resorption during periodontal wound healing. J Clin Periodontol 1984;11(1):41-52. 6. Nyman S, Karring T, Lindhe J, Planten S. Healing following implantation of periodontitis-affected roots into gingival connective tissue. J Clin Periodontol 1980;7:394-401. 7. Gottlow J, Laurell L, Lundgren D, et al. Periodontal tissue response to a new bioresorbable guided tissue regeneration device: a longitudinal study in monkeys. Int J Periodontics Restorative Dent 1994;14:436-49. 8. Sallum EA, Sallum AW, Nociti FH Jr, Marcantonio RA, de Toledo S. New attachment achieved by guided tissue regeneration using a bioresorbable polylactic acid membrane in dogs. Int J Periodontics Restorative Dent 1998;18:502-10. 9. Blomlöf L, Lindskog S. Cervical root resorption associated with
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