Human suprabony healing responses following root demineralization and coronal flap anchorage Histologic responses in 7 sites S. S. Stahl and S. Froum Department of Periodontics. College of Dentistry, New York University, 345 East 24th Street New York, NY 10010 New York. New York 10010. USA Suihl SS ami Frown S: Human suprabony healing responses following root demineralization ami coronal tltip anchorage. Histologic responses in 7 Sites. J Clin Periodontol 1991: IS: 685 689. Abstract. 6 suprabony pockets in 2 adult patients were treated with debridement and citric acid root demineralization. Following these procedures, coronal positioning of the marginal flaps was performed at 2 sites. At 4 sites, the marginal flaps were sutured coronally using orthodontic brackets as anchors. At 1 additional site, root debridement only was performed and the margin was placed at aboui crestal Level. Prior to root planing, all roots were notched both at the level of the gingiva! margin and the most apically positioned calculus, Blocks were harvested 7 and 18 weeks postsurgen and prepared for histologic analysis. Clinical results showed a gain in probing attachment in both coronally positioned sites (average= 1.8 mm) and cororally anchored sites (a\erage = 4.5 mm). The additional debrided-only site showed a gain in probing attachment of 0.1 mm. Histologically. new cementum with functionally inserted fibers was seen within the calculus notch in all coronally anchored sites. This new attachment was associated with crestal osteogenesis. In the 2 coronally positioned and root demineralized sites, new attachment was seen within the calculus noich in 1 out of the 2 specimens evaluated. Within the limits of the evidence presented, coronal anchorage of Maps enhanced probing attachment and new attachment when used in conjunction with root demineralization. Key words: root demineralizaiion and flap anchorage. Accepted for publication 21 August 1990 In a recent publication (Stahl & Froum 1991), we reported on histologjcallj observed new attachment in suprabony lesions treated b> a combination of debridement. GTR and coronall\ anchored flap procedures. Such new attachment was not observed in parallel sites in which only coronally anchored flaps and debridement were employed. To further evaluate the efficacy of coronal anchorage of the gjngival margin, we are now reporting on histologic healing responses in human suprabony lesions in which debridement. coronal Hup anchorage and root deminerali/ation This study was supported in part by the Claire anil Melvyn Kaufman Institute for pL'riodontiil Research, New York University College ill' Dentistry. New York. Now York. USA. were utilized. These evaluations were stimulated by the recognition that one of the variants determining success or failure of new attachment is the "degree of gingiva] recession that occurs during healing'" (Gottlow. et al. 19X6) and the clinical successes reported in bone fill of furcation involvements when coronal anchorage was employed as part of therapy (Martin et al. I9N8, Gantes et al. 1988, Garret et al. 1990). In fact, the combination of crown anchorage and root demineralization in the treatment of furcation lesions appeared as effective in obtaining bone fill as when additional enhancing procedures such as bone grafts or collagenous membranes were used (Garret et al. 1988, 1990). Material and Methods Clinical and histologic responses at 7 suprabony lesions in anterior teeth of 2 volunteer patients (1 male (patient no. 1). and 1 female (patient no. 2n are included in this report. These patients were 55 and 56 years-old, respectively. Both patients were in good health and each signed an informed consent following explanation of the study, and providing freedom to withdraw at the patient's will. Surgery was performed as part of the overall periodontal treatment plan in the Department of Periodontics. New York University. College of Dentistry. The 7 leeth selected had been scheduled for extraction for periodontal reasons by 2 periodontists, not a part of this study. Prior to surgery, cause-related therapy was performed as necessary. However, root planing at the sites to be evaluated was performed only after the root was notched al time of surgery. Root debridement was performed by 686 Suihl t(J Frown Fig, I. Clinical a p p e a r a n c e o f d e b r i d e d sites with facial b r a c k e t s , patient no, 2, teeth ••! I a n d 21 open debridemenl using an ultrasonic sealer and hand instrument until all visible calculus was removed. Hoih magnifying lenses and fiber optic light were employed to detect calculus. Pre-treatinent photographs and radiograms were taken at this time and photographs were obtained during surgerj lor clinical documentation. In addition. 4 teeth (patient no. 2) included in this study had orthodontic brackets bonded to the facial surfaces of these teeth 2 weeks prior to surgical therapy. Measurements Immediately prior to surgery, a horizontal notch WLIS made on the facial root surface at the level of the gingival margin using a 1/2 round bur. To insure reprodueibility at subsequent measurements, a vertical notch was placed in the crown of each tooth to guide the silver point used for measurements. All measurements were made to the nearest 0.1 mm using a number 50 silver point, a locking plier and a Boley gauge. The h'ii;. 2. Clinical a p p e a r a n c e of d e b r k i c i l silcs with facial b r a c k e t s , patient n o . _, Led 41. and distance from the gingival notch to the base of the clinical pocket was recorded prior to surgery and I week prior to block section. At the time of surgery, and prior to root planning, a 2nd notch was made through the most apical level of visihle calculus and the distance from the calculus notch to the osseous crest was measured. The notching accuracy of the visible calculus was optimized in these sites, since ihey were at facial surfaces of anterior teelh and therefore clearly visible to the operator (SF). Surgical procedure An inlrasulcular incision was made to elevate a full/split thickness mucoperiosteal flap in order to retain as much marginal gingiva as possible. The apical split thickness procedure allowed for coronal stretching. After root/calculus notching, the root was thoroughly debrided and the measurements described above recorded. At 6 facial sites. a rubber dam was placed. After placemenf of the dam, citric acid. pH 1, was applied to the root surfaces for 3 min using a cotton pellet to rub the acid into the root surface. At 2 sites (patient no. 1. teeth •i-22. 23). the Haps were sutured coronally. At 4 sites (patient no. 2. teeth -11. 21, 31. 41) the flaps were anchored coronally by suturing to the facial orthodontic brackets (Figs. I, 2). Interrupted sutures of 4.0 silk or Dexon were utilized at all sites. No dressing was placed. At 1 site, (patient no. 1, tooth s l l . root debndement only was performed and the flap was sutured at about the cresial level. Patients were instructed to rinse with 0.12% chlorhexidine gluconatc 2x a day for 2 weeks. Flap sutures were removed 2 weeks following surgery. Patients returned lor professional plaque removal every 2 to 3 weeks until the blocks were harvested. Block sections were removed at 7 and 18 weeks after surgery. At the lime of block removal, clinical records, photographs and radiographs similar lo those described at initial surgery were taken. After block removal, teeth were fixed in 10% buffered formalin, decalcified in FDTA and embedded in paraffin. Step serial sections 8 // thick were cut and stained for histoiogic evaluation using routine histoiogic stains. Results Clinical Observations (Table 1) Pertinent clinical findings are reported in Table I. Summarizing these obserRoot demineralization and coronally anchored /laps 687 Vtibk' 1. Rool demineralizalion ;md coronal tl.ip placemenl Pattern no. 1 3 Tooth 22 2.1 I 21 31 4 II Procedcor. posil. cor. anchor liebr. only Preop P.D. (mm) 7.0 5.0 6.6 6.(1 12.2 7.0 6.0 Observation time 1 weeks) 7 18 IS 18 18 7 Post op. CD. unm.i 1.2 1.2 i s 2.0 2.1 3.0 Recession mi ml 1.5 2.1 1.2 I.I' 3.5 1.2 2.9 Gain in probing attach. (mm) 1.8 1.7 N.A. 4.2 N A. 3.2 N.A. 6.7 N.A. 3.7 N.A. ( I . I N.A.: New attachment. \ations, we noted lhat the average preoperative pocket depth at the 6 sites receiving root demineralization was 7.3 mm (5.0 inin 12.2 mm). Following surgical procedures, the average postoperative pocket depth was 2.0 mm (1.2 mm-3.6 mm). Recession averaged 1.8 mm (1.0 mm-3.5 mm) and gain in probing attachment averaged 3.6 m m (1.7 mm -6.7 mm). The debrided-only site (patient no. 3, tooth II) showed a preoperativc pocket depth of 6.0 mm and a postoperative pocket depth of 3.0 mm. Recession was 2,9 mm and the gain in probing attachment \\;is().l mm. Observation time was 7 weeks. In comparing specific gain in probing attachment between coronally-placed and coronally-anchored sites, we noted Fig. 3. Overview of root surface coronal to calculus notch at tooth ((31 in patient no. 2. IS weeks after surgical procedure. Hemaloxylin- eosin slain. Note root surface resorption apical to junetiona! epithelium. Arrow points to apical position of J E that the average gain in probing attachment following coronal positioning was 1.8 mm (1.7 mm—1.8 mm), while gain in probing attachment following coronal anchorage averaged 4.5 mm (3.2 mm 6.7 mm). No untoward clinical responses were recorded at any treated site during the entire observation period. Histologic observations (Table 1) The site treated by debridement and marginal placemenl at crest level (patient no. 3) showed closure by epithelial adhesion at a root site apical to the calculus notch. The sites treated by debridement. root demineralization and coronal flap positioning showed varying healing responses. At I site, the gingival margin had receded apical to the calculus notch and closure was by epithelial adhesion. At the other site (patient no. I, tooth -23). the calculus notch showed epithelial adhesion in its' coronal portion. At the apical portion of the notch, the dentin surface demonstrated both deposition of repair cementum with inserted collagen libers and surface dentin resorption in the presence of odontoclasts. Thus, within this calculus notch, both dentin resorption and new attachment were present 7 weeks after procedure. Such responses apparently limited the apical migration of the junctional epithelium to the coronal portion of the calculus notch at the time of block section. The sites treated with debridement. root demineralization. and coronal Hup anchorage demonstrated new attachment within the calculus notch at all 4 sites examined. At one site (patient no. 2. tooth =31, 18 weeks postsurgery), the gain in probing attachment of 6.7 mm was reflected histologically by new attachment within the calculus notch and root surface resorption coronal to the calculus notch (Figs. 3. 4). Thus, as seen at 7 weeks postsurgery. combinations of both regeneration and root surface resorption was also observed at 18 weeks after surgery within the same site. Again, these responses limited the apical migration of the junctional epithelium. At other calculus notch sites where the coronal anchorage was employed, new attachment was seen within the apical portions of the calculus notches. New attachment was visualized by deposition of cellular (repair) cementum with attached fibers present on the dentin surface of the notch (Figs. 5. 6). Within the calculus notches and coronal to the new attachment, connective tissue often lined the dentin and extended to the level of epithelial adhesion. New attachment responses were also associated with varying degrees of crestal osteogenesis in all observed specimens. It should be noted that site serial sections demonstrated variations in extent of the histologic responses described above. However, the regenerative responses depicted were present in the great majority of serial sections within each site. Fig. 4. She o( calculus noich in specimen shown in Fig. 3 (25 x ). This was located apically to rool surface resorption. Note osteogenesis. eementogenesis and oriented PDL fibers (new attachment) within the calculus nolch. 688 Smli! <$ Froum Fig. 5. Overview of calculus notch in tooth all. patient no 2, is weeks after surgical procedures. Hematoxylin-eosin stain. Note new attachment in apical portion of notch facing the supracrestal gingival unit. Arrow points to apical position of J E. Discussion Previous studies from our department reported on closure by epithelial adhesion following root deminerali/ation in human suprabony lesions without evidence of new attachment iStahl & Froum 1977. Kushaui et al. 1984). Conu s' • * • • * . . • % k • v HMHi mwk Fig. 6. Higher magnification of new attachment site shown in Fig. 5 (Mtign. 25 x). Cellular cementom is deposited on dentina] wall and libers are attached to thecementum. trary to those observations, the responses observed in the present material are similar to those reported in human periodonlal lesions by Cole el al. (1980). who described new attachment following debridement and root demineralization in 10 treated surfaces. Furthermore, our present histologic results also Mipport the clinical observations that reduction in marginal recession during the early stages of Hap healing enhances gain in probing attachment (Martin et al. 1988, Gantes el al. 1988). Of special interest in the present material is the odontoclaslic activity (root surface resorption), seen at both the 7 and 18 weeks postsurgery interval. Root surface resorption may well be a response to root dermneralization. On the other hand, it may be part of a regenerative phenomenon, since it has been observed following techniques other than root demineralization (Karring el al. 1984. Magnusson et a!. 1985). Surface resorption may also be due to contact between gingival connective lissue and root surface, which may be enhanced by coronal flap anchorage (Kamng et al. 1980). Obviously, from the material at hand, we cannot identify the specific etiology of root surface resorption in these cases, nor can we predici the ultimate extent of such resorption. However, it may well be limited, since extensive root resorption. such as that observed with the use of marrow grafts, has noi been reported following the regenerative procedures discussed above. On a positive note, root surface resorption appear to limit migration of (he junctional epithelium. Such limitation may be due 10 the linkage between deniinal collagen and wound surface collagen which has been reported to occur as early as 7 days following surgery and root demineralization (Garret et al. 1978. Selvig et al. 1981, 1988. Frank et al. 1983). Finally, let us compare clinical and histologic healing responses in human suprabony lesions when either coronal anchorage and barrier membrane or coronal anchorage and root demineralization was used. Such a comparison shows similar histologic responses with both techniques, namely a pronounced tendency toward new attachment at root sites previously covered by plaque and calculus. Gain in probing attachment appeared similar when either coronal anchorage and barrier membrane (averagegain: 1.7 mm i or coronal suturing and root demineralization was employed (average gain: 1.8 mm). However, gain in probing attachment appeared enhanced when coronal anchorage and root deminerali/ation was used (average gain: 4.5 mm). Since, histologically. the root surfaces apical to the notch demonstrated both cemental deposition and resorption. length of newly deposited cementum could not be measured accurately in these specimens. As we compare our results, words of caution are necessary. First, the number of sites we studied histologically are, of necessity, extremely limited. Therefore, they do no( permit statistical projections of significance. Second, results were not site predictable. However, the tendencies toward regeneration, seen histologically with techniques using barrier membranes, root demineralization or bone grafts, are encouraging. In addition, the control of marginal shrinkage during the early healing stages may also play an important role in enhancing regeneration of lost attachment (Garreti etal. 1990). Zusammenlassung Mensehliche, mpraossare Heilungseffekle nach WurzeldemineruiisQlion und koronaler Lappenverankerung. Histologische Antworten tin 4 Stellen Bei 1 erwachsenen Patienten wurden 6 snpraossiire Taschen mil Konkremcnlentfernung und Wurzeldemineralisation dureh Zitronensaure bchandelt. Nach diesen Behandlungssequenzen wurden die tnarginalen I appen an 2 Stellen koronal befestigt An 4 Slellen wurden die margmalen Lappen koronal mil Suturcn vcrschen und durch ortbodontische brackets verankerl. An ciner zusilzlichen Sidle wurden ausschliesslich Konkremente entfernt und der Zahnfteischrand etwa in der Hohe des Knochenkammniveaus befestigt. Vor der Wur/dglatlune wurden in Hone des Zahnfleischniveaus und der am weitesten apikal vorkonimendcn Zahnsteinkonkremente, Wurzeikerben angebracht. 7 und IK Wochen nach dum chiiurtiischen liingriff wurden Gewebeblocks entnommen und zur histologischen Analyse vorbereitel. Die klinischen Resullate zeiglen einen Gewinn sondierten Attachments bei snwohl den koronal befestigten (Mittdweri= l.S mm) als ;iuch den koronal verankerlen SleSlen (Mittelwert= 4.5 nun). Bei der zusatzlichcn, ausschliesslich depurierten Stelle wurde ein Attachntentgewinn von O.I mm beobachtet. An alien Stellen mil koronal verankerten Lappen zeigtc das histologische Bikl neugebifdetcn Zenient mit lunktioneli onentierten Fasern innerhalb der Zahnsteinkerbcn. Dieses neugebildete Atuehment war mil osleogenetisclien Vorgangen in deralveolaren Knochenleisle vergeseUschaftet. Bei den bei den koroiiLiI befestigten und wurzeldemineraRoot demineraiization and coronally anchored Slaps 689 lisierten Stellen wurde bei 1 der 2 untersuch- •on Priiparate neugebildetes Attachment innerhalh der Zahnsteinkerbe beobachtet, Die hior angegebencn, begrenzter Aussagen zeigen, d.iss die koronale Lappen^erankerung Jus sondierbare Attachment so\ue die Neubildunj; von Attachment verbesserte, wenn gleichzeitig die Wurzeln demineralisierl wurden. Resume Gueri.ion supraosseuse htanairu ••uite a la demineralisation radiculaire ci tmcrage coronaire Ju latnheau. Reponses kislologiques an niveau de sepi sites (> poches supraosseuses the? deu\ adultes ont etc trances pur lissage radiculiiiic L-I demineralisation rudieulaire a t'acide cnriquc. Les lambeaux on1 ensuite ete positionnes en coronaire au niveau de deux sites, Les lambeaux marginaux ont ete sutures en coronaire a I'aidc de brackets d'orthodontie uiihscv comme ancrage au niveau de qu.ure .iutres sites. Aii niveau dun autre sile, seul un lissage radiculaire a ete elTectue et la gencive placet au niveau de la crete osseuse- Avant le lissage i.nliiulaiii.'. mutes les racines ont cie cnlail- IOL-S au niveau de la gencive marginalc ainsi qu'a celui du lartre le plus apical- Des biopsies ont ete obtenues 7 et 18 semaines apres I'operation ct preparees pour I'analyse histologique. Les resultats climques onl montre un gain d'attachc au sondage tarn au\ sites positionnes en coronaire(moyenne = 1.8 mm) qu'aux sites ancres en coronaire (moyenne = 4.5 mm). Le dernier site n'avail qu'un gam de 0.1 mm. Du nouveau cemenl avec fibres inserees -i ete trouve dans fentatlle sous le lartre dans tous les sites ancres en coronaire. Celte nouvtUe attache; eiait accompagnee d'osteogenese erestale. Scul un des deux sites positionnes en coronaire avail une nouvelle attache conjunctive duns I'entaille sous le tartre Malgre le nombre reslreint dc sites analyvi.--. il semblerai! qu'un ancrage en coronaire des lambeaux associe a la demineralisation radiculaire. augmenle 1'attache conjonctive. References Cole. R. T.. Criggcr. M., Bogle, G., Egelberg, J. & Selvig, K. A. (1980) Connective tissue regeneration to periodorilally diseased teeth. Journal of Periodontal Research 15. 1-9. Frank. R. M.. Fiore-Donno. G. & Cimansoni. G. (1983) Cememogenesis and soft tissue altachmeni after citric acid treatment in a human. Journal of Periodontology 54, 389-401. Gantes, B.. Martin, M.. Garret. S. & Egelberg, J. (1988) Treatment of pcriodontal furcation defects (II). Bone regeneration in mandibular Class II defects. Journal of Clinical Periodontology 15. 232-239. Garret, J. S., Crigger, M- & Egelberg. J (1978) Effecs of cilric acid on diseased root surfaces. Journal of Periodontal Research 13, 155-163. Garret. S , Loos, B.. Chamberlain. D. & Egelberg. J. (1988) Treatment of intraosseous periodontal defects with a combined therapy of citric acid conditioning, bone grafting and placement of collagenous membranes. Journal of Clinical Periodontology 15, 383-389. Garret, S.. Martin, M. & Egelberg, J. (1990) Treatment of periodontal furcation defects. Journal of Clinical Periodontology 17. 179-185. Gottlow. J.. Nyman. S., Lindhe, J., Karring. T. & Wernstrom. J (1986) New attachment formation in the human periodontium by guided tissue regeneration. Case reports, Journal of Clinical Periodontology 13. 604-616. Karring, T., Nyman. S. & Lindhe. J- (1980) Healing following implantation of periodontally affected roots into bone tissue Journal of Clinical Periodontology 7. 96-105. Karring. T., Nyman, S.. Lindhe, J. & Sirirat. M. (1984) Potential for root resorpiion during periodonial healing. Journal of Clinical Periodontology El. 4 1 - 5 2 . Kashani, H. G.. Magner, A. W. & Stahl, S. S. (1984) The effects of root planning and citric acid applications on flap healing in humans. Journal oj Periodontologj 55, 679-683. Magnusson. I., Claffey. N.. Bogle. G.. Garret. S. & Egelberg. J. (1985) Root resorption following periodontal flap procedures in monkeys. Journal of Clinical Periodontohgy 20. 79-85. Martin, M,. Gantes. B.. Garret. S. & Egelberg. J. (1988) Treatment of periodontal furcation defects (I). Review of the literature and description of a regenerative surgical technique. Journal of Clinical Periodontoiogy 15. 227 231. Selvig, K. A., Riric. C. M.. Nilveus, R. & Egelberg. J. (1981) Fine structure of new connective tissue attachment following acid treatment of experimental furcation pockets in dogs. Journal oj Periodonial Research lh. 123 129. Selvig. K A.. Bogie. G. & Claflev. N. M. (1988) Collagen linkage in periodontal connective tissue reattachment. Journal of Penodonlotogy 59. 758-768. Stahl. S. S. & Froum. S, J. (1991) Healing of human suprabony lesions treated with guided tissue regeneration and coronally anchored Haps, Case reports. Journal of Clinical Periodontology 18. 69-74. Stahl, S. S. & Froum, S J- (1977) Human clinical histologic responses following the use of citric acid in periodontal therapy Journal oj Periodontology 48. 261-268. Address: S. S. Siahl Department of Periodontics College oj Dentistr) New York University 345 Earn 24sh Street New York. NY 10010 USA