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II. 13 to 18 Months
S. J. Froum and S. S. Stahl
Accepted for publication 14 March 1986
FIVE INTRABONY LESIONS IN A 40-year-old healthy, white female patient suffering with severe periodontitis were removed en bloc, 13 to 18 months after flap debridement and graft placement. At the time of debridement, the position of the gingival margin and the most apically located calculus were notched in the root to serve as reference points. All lesions received tricalcium phosphate ceramic implants, and the lesions healed uneventfully. The sites were professionally cleaned frequently during the experimental period. At the time of block removal, clinical measurements demonstrated gingival recession (average = 2.6 mm) and a gain in clinical closure (average = 2.3 mm). Histologic evaluation of step serial sections of these blocks showed limited presence of graft particles. The particles were surrounded by dense connective tissue. They did not induce inflammation, nor did they appear to enhance osteogenesis or cementogenesis. Closure of lesions was essentially done by a long junctional epithelium adhesion and limited evidence oi' new connective tissue—root attachment. In the 18-month specimen, active root resorption was seen immediately apical to the junctional epithelium at a site demonstrating significant inflammation in some sections. Fibrils apparently arising from the resorbing dentinal wall were seen in these sections. Serial sections of this site showed cellular cementum and functional fiber attachment at the resorption sites. These variations in resorption/repair/ regeneration within the same surgical site were seen 18 months postsurgery and thus may reflect local tissue responses to inflammatory fluctuations rather than surgical sequellae. In a recent report, we reviewed the pertinent literature and described human intraosseous healing responses to tricalcium phosphate ceramic implants over an 8-month period.1 We now wish to briefly extend these observations to 13 to 18 months after graft placement, again using clinical and histologic parameters for our evaluation.
MATERIALS AND METHODS
Five periodontal lesions in a healthy 40-year-old female volunteer patient were selected for histologic study of the effects of tricalcium phosphate, ceramic implants in the repair of intraosseous lesions. These sites were diagnosed as having a hopeless periodontal prognosis by the dental treatment team, and the patient signed an informed consent as part of the protocol requirements. Roots at the involved sites received a notch at the gingival margin which served as a reference for pocket measurements to within 0.1 mm. The notch was created using a half-round bur. After obtaining local anaesthesia, a full-thickness mucoperiosteal flap was elevated. Prior to debridement. and again using a half round bur, the root was notched through the most apical extension of calculus. The lesion was then thoroughly debrided and appropriate measurements taken. Following intramarrow penetration, the site was overfilled with the ceramic graft material. The flap wall was then positioned as incisally as possible and complete closure was attempted. Interrupted sutures (4.0) were used and a periodontal dressing was applied over the sutured site.
*Departmcnt of Periodontics, New York University College of Dentistry, New York.. NY. This study was supported in part hy a Grant-in-Aid from the Johnson and Johnson Dental Products Co.. Fast Windsor. NJ 08520.
†The graft material is marketed as "Synthograft" by Johnson and Johnson Dental Products Co.. East Windsor. NJ 08520.
All presurgical and immediate postsurgical measurements and photographs were taken during this time. Ten days after graft placement, dressings and sutures were removed and the site cleansed. Then, the patient received weekly professional plaque removal at the surgical site for the first 6 weeks and then once every 2 to 4 weeks until the block was removed.
Figure 1. Preoperative appearance of implant sites, teeth #12 and 13.
Figure 2. Preoperative radiogram of sites, teeth #12 and 13.
At time of block removal, appropriate clinical records, photographs and radiograms were taken, and pocket depth, recession and the amount of clinical closure were recorded, again using the gingival marginal notch as the fixed point of reference. Blocks were removed 13 to 18 months after graft placement.2-3 No adverse reactions were noted during the observation time. Upon removal, all specimens were decalcified and prepared for histologic study. Step-serial, mesiodistally cut sections were prepared and selectively stained with hematoxyhn-eosin, Mallory-Trichrome and Van Kossa stains.
Clinical Observations (Table 1)
Preoperative pocket depth at the five sites ranged from 8.5 mm to 13.2 mm and intraosseous depth ranged from 3.2 mm to 8.7 mm.
Figure 3. Sites debrided, teeth #12 and13.
The osseous configurations were essentially one- to two-wall lesions. Following treatment, the sites showed pocket depth ranging from 4.3 mm to 7.2 mm. Gingival recession was present at all sites and ranged from 1.9 mm to 3.0 mm. Clinical gain in closure ranged from 1.7 mm to 3.0 mm (Figs. 1-9). All measurements were made from a fixed point (marginal notch) using an endodontic silver point and Boley gauge to measure distances to the nearest 0. 1 mm.4
Histologic Observations
In the five sites available for histologic evaluation, the gingival margin had receded apical to the marginal notch. Closure was by adhesion of the junctional epithelium (JE) to the level of the most coronal fiber/cementum insertion sites. Inflammation at these pocket sites varied from minimal to severe in both inter- and intraspecimen comparisons but did not seem to be related to the presence or absence of graft particles. Our specimens showed minimal presence of graft particles at the operative sites.
Figure 4. Ceramic implants tn place at sites, teeth #13 and 14.
Figure 5. Postoperative appearance of implants sites, 13 m, postsurgery.
Figure 6. Postoperative radiogram of implant sites teeth #13 and 14. 13 m. postsurgery. Note notches in root placed at time of surgery.
However, around the still remaining particles, inflammation was minimal or absent and dense connective tissue bundles surrounded the implants.
Figure 7. Preoperative appearance of implant site, tooth #3.
Figure 8. Preoperative radiograms implant site. tooth #3
Our specimens showed no evidence of osteogenesis at particle seams and the alveolar crest was remodeling (Figs. 10 and 1 1). Cemento-dentoclastic activity was seen at the root surface below the most apical position of the JE in one specimen (mesial, tooth #3). The resorbing site demonstrated odontoclasts, and the connective tissue at this site was highly cellular (Figs. 12-14). Fibrils appeared to project from the dentin border and were at right angle orientation to the dentinal wall. These fibrils stained as collagen (Fig. 15). In step serial sections of this site, areas of surface root resorption were seen at the level of the JE (Fig. 16). Here, the coronal cemental resorption area was covered by the migrating junctional epithelium. Immediately apical to this epithelial adhesion, cementogenesis had taken place at the resorption site and functionally attached fibers inserted into this cellular (repair) cementum (Figs. 17-18). The epithelial migration appeared to be limited by the fiber insertion. Obviously, we have no information when the cemental/dentin root resorption and epithelial adhesion/cementogenesis occurred.
Figure 9. Postoperative radiogram of implant site, tooth #3, 18 months postsurgery. Note notches in root placed at time of surgery.
Figure 10. Histologic overview of implant site, tooth #13 (magnification x 10)
However, the process took place apical to the most apical position of calculus (notch) and within the surgical site.
Comment
As in the earlier report, the present data do not indicate significant (1) new attachment, (2) cementogenesis or (3) osteogenesis in healing periodontal lesions in the presence of ceramic implants harvested 13 to 18 months after placement. Of interest in our blocks was the paucity of graft particles remaining at the operative sites.
Figure 11. Higher magnification of implant site shown in Figure 10. Note connective tissue surrounding implant particle site (arrow) (magnification x 64).
Figure 12. Histologic overview of root resorption site, tooth #3, mesial (magnification x 10)
While the specific reason for the limited presence of particles could not be determined, it may reflect resorption or exfoliation of these particles with subsequent replacement by dense connective tissue at this time interval. Of particular interest was the presence of root resorption about the most apical positions of the junctional epithelium.
Figure 13. Serial section of resorption site shown in Figure II (magnification x 25).
Figure 14. Higher magnification of root resorption site shown in Figure 13. Note odontoclastic activity (magnification x 160).
Figure 15. Higher magnification of root resorption site in tooth #3. Note fibrils at dentin border (arrow) (magnification x 160).
Figure 16. Serial section of root resorption site shown in Figure 12, tooth #3. Note root resorption limited to cementum and JE migration into these resorption bays. The migration appears to be limited by cementogenesis immediately apical to the JE (magnification x 10),
Figure 17. Higher magnification of Figure 16. Note interface between JE and new cementum (magnification x 25).
Since such cemental/dentinal resorption patterns have been observed following ceramic graft placements.1 subgingival placements of crowns5 and experimental periodontal flaps in cats,6 the observed root resorption cannot be solely the result of placement of ceramic grafts. Rather, it may reflect root responses to inflammation at sites of local injury.7-9 The sequellae to cemental resorption is loss of fiber attachment, thereby allowing migration of epithelium onto this fiber-denuded root. Or, if resorption extends into surface portions of dentin, it may unmask dentinal collagen which in turn may link with gingival fibers to create attachment at this site with subsequent mineralization of the resorption site.10-12 On the other hand, the severity of inflammation may lose all fibrils, thereby allowing for epithelial migration onto this root site.13-14 In this connection, a recent report of healing responses following flap surgery in dogs described resorption lacunae at the dentin surface two weeks after surgery. Electron microscopic studies of the resorption sites noted that "in these sites, interdigitation of newly formed collagen fibrils with denuded ones on the resorbed dentin surface was observed."15 Finally, root resorption has also been related to early postsurgery sequellae when gingival connective tissue contacted denuded dentin.16 On the other hand, periodontal ligament cells coming in contact with the root surface, possessed the ability to "reestablish connective tissue attachment."17 Our specimen showed active root resorption taking place 18 months after surgery.
Figure 18. Higher magnification of Figure 16. Note functional attachment of fibers into areas of "new cementum" (magnification x 64)
Thus, as pointed out previously, root resorption may not be limited to early postsurgical sequella but may also reflect cementum-dentin responses to on-going inflammatory shifts within periodontal lesions. When such resorption sites become exposed to the oral environment, they may predispose to plaque and calculus retention and possibly relate to increased root caries seen in patients with higher periodontal disease scores.18
REFERENCES
1. S. Stahl. S. S.. and Froum, S.: Histological evaluation of human intraosseous healing responses to the placement of tricalcium phosphate ceramic implants—I. Three to eight months. J Periodontol 57: 211,
2. Dragon. M. R,. and Sullivan. H. C: A clinical and histologic evaluation of autogenous iliac bone grafts in humans. J. Periodontol 44: 599, 1973.
3. Froum, S. J.. Thaler. R.. Scopp, I. W.. and Stahl. S. S.: Osseous autografts—II. Histologic responses to osseous coagulum—Bone blend grafts. J Periodontol 46: 656. 1975.
4. Froum. S. J.. Thaler. R.. Scopp. I. W., and Stahl. S. S.: Osseous autografts —I. Clinical responses to bone blend and hip marrow grafts. J Periodontol 46: 515. 1975.
5. Stahl. S. S.and Tarnow. D.: Root resorption leading to linkage of dentinal collagen and gingival fibers? J Clin Periodontol 12: 399, 1985.
6. Tal, H.. and Slahl. S. S.: Periodontal attachment responses to surgical injury in the cat. J Clin Periodontol, in press (1986).
7. Stahl, S. S.. and Tonna. E. A.: Comparison of gingival repair following chemical or surgical injury. Periodontics 6: 26. 1968.
8. Andreasen. J, O., and Hjoning-Hansen, E.: Replantation of teeth. II. Histologic study of 22 replanted anterior teeth in humans. Acta Odontol Scand 24: 287, 1966.
9. Aukil. I., Simpson. D. M. and Schaberg, T. V.: An experimental study of new attachment procedures in beagle dogs. J Periodont Res 18:643, 1983.
10. Selvig, K. A., Prie. C. M.. Nilveus. R.. and Egelberg. J.: Fine structure of new connective tissue attachment following acid treatment of experimental furcation pockets in dogs. J Periodont Res 16: 123, 1981.
11. Frank. R. M., Fiore-Donnot. G., and Cimansoni, G.: Cementogenesis and soft tissue attachment after citric acid treatment in a human, an electron micrographic study. J Periodontol 54: 389, 1983.
12. Hertier. M: Ultrastructural study of new connective tissue attachment following application of phosphoric acid on human root dentin. J Periodontol 54: 515. 1983.
13. Stahl. S. S.: Speculation on periodontal attachment loss. J Clin Periodontol, in press (1986). 14. Stahl, S. S.: Periodontal attachment in health and disease. J West Soc Periodontol, in press (1986).
15. Noguchi. Y.: Ultrastructural study on the new attachment between surgically denuded dentin surfaces and regenerated peroodontal tissues (Abstr. No. 3). J Jpn ASSOC Periodontol 26: 1984, 16. Kaaring, T., Nyman. S., Lindhe. J., and Sirirat, M.: Potentials for root resorption during periodontal wound healing. J Clin Periodontol 11:41, 1984.
17. Nyman, S., Gottlow, J., Karring. T.. and Lindhe, J.: The regenerative potential of the periodontal ligament. J Clin Penodontol 9:257, 1982.
18. Banting, D. W.. Ellen, R. P., and Fillery, E. D.: A longitudinal study of root caries, baseline and incidence data. J Dent Res 64: 1141, 1985.
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