Healing of human suprabony lesions treated with guided tissue regeneration and coronally anchored flaps Case reports* S. S. Stahl and 5. J. Froum Department of Penodontics, College of Dentistry. New York University. New York, New York, USA Siahl SS nut! Froum S.I. Hailing of human suprabony lesions treated with guided /issue regeneration and coronally anchored flaps. Case reports. J Gin Periodontoi 1991; 18: 6V-74, Abstract. Teflon membranes were interposed between soft tissue flaps and roots in 4 human suprabony lesions affecting the mandibular incisor teeth in 1 volunteer patient. 4 suprabony lesions affecting the mandibular incisor teeth were used as comparisons in a 2nd patient. All roots were debrided using ultrasonic and manual instruments and the most apical positioned calculus site on the facial surface was notched. Flaps were suiuivd as coronally as possible using orthodontic brackets as anchors. Tissue blocks were removed 2 to 3 months after procedures and the facial aspects ol' all teeth were examined histologically. New attachment in the form of new "cenientum with functionally oriented fibers" was seen within the calculus notch in 3 out of 4 membrane-treated sites and immediately apical to the notch at 1 site. The 4 comparison sites showed no evidence of new attachment within or adjacent to the notch. Rather, the gingival margins were located apical to the notch. Our observations suggest that guided tissue regeneration techniques improved coronal attachment responses in human suprabony lesions within the sample described. Key words: guided tissue regeneration: coronally anchored (laps Accepted for publication 10 January 1990 Histological evaluation of human responses to the use of guided tissue regeneration (GTRi techniques have focused essentially on intrabony and furcation sites (Nyman et al. 1982, Gottlow et al. 1986, Becker et al. 1987, Stahl et al. 1990). Al these sites, new- attachment in the form of new cementum with functionally oriented fibers was histologicalK observed on root surface previously exposed to the oral environment. While the above-cited repons have shown positive responses using guided tissue regeneration in human furcation and intrabony sites, limited evaluations are currently available which describe histologic responses with the use of GTR techniques at suprabony sites. The present paper will ad- * This study was supported in purl by a gninl in aid from the Claire and Melvyn Kuulrn;in Institute For Periodontal Research. New I'lmersily, ColL-iie ot Dentistry dress such responses using human histologic case reports. In addition, recent reports have depicted chemical root treatment and coronal flap replacement to be associtated with gains in clinical closure and osseous fill in molar furcation lesions (Gantes et al. 1988). Since an interposed membrane may maintain necessary space for coronal migration of progenitor cells in suprabony lesions (Gottlow et al. 1986), the coronal anchoring of gingival tissues could maximize new attachment at such sites. Thus. the present case reports attempted also to histologically evaluate healing responses ai -^iprabony sites when flap margins were anchored coronally. Material and Methods 8 suprabony lesions at 8 mandibular incisor teeth were treated in 2 male volunteer adult patients. These patients were 27 and 51 years-old respectively. Treatment consisted of open debridement flap procedures followed by coronal anchoring of the gingival margins. At 4 sites, a membrane barrier* was inserted prior to flap closure. Both patients were in good health and each signed an informed consent following explanation of the study and providing freedom to withdraw at the patients will. Surgery was performed as part of the overall periodontal treatment plan in the Department of Periodontics. New York University. College of Dentistry. Ail 8 teeth selected had been scheduled for extraction for periodontal reasons by two periodontists not part of the 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 at time of surgery. * Gorctex membrane manufactured by W. L. Gortex Assoc. Inc. Fliigsia/T, AZ. USA. 70 Siahl & Froum lruioil appearance of patient no. I Fig. 2. Flaps retracted, patient no. 1. Fig. 3. Membranes being placed, patient m>, I Fig. 4. Flaps coronally anchored, patient QO. I Fig. 5. Flaps rL'iracied. pattern no. 2. Root debridement was performed hv open debndement using ultrasonic sealers and hand instruments until all visible calculus was removed. Both magnifying lenses and liber optic light were employed to dctcci calculus. Pre-trcatmerit pnoiographs and radiograms were taken at tins time and photographs were obtained during surgery for clinical documentation. Measurements All teeth included in the study had orthodontic brackets bonded to the facial surfaces of the teeth I to 2 weeks Guided tissue regeneration and coronally anchored flaps 71 Table 1. branes Pi no. I average: Table 2, Pt. no. 2 average: Clinical Age (years) 51 Clinical Age (years) 27 responds to Tooth site (BU) 32 4 42 responses to Toolh site (BUI 12 31 41 42 the use ot debridemen Preop. P.D. (mm) 6.0 5.7 4.2 5,2 5.3 Experiment time (weeks) 8 8 8 8 the use of debndemenl Preop. P.D. (mm) 7 0 5.0 6.2 5.9 Experiment time 1 .UVkst 12 12 12 12 [. corona] anchoring and Poslop. PD. (mm) 4.0 3.7 L5 2.3 2.9 and coronal Postop. P.D. (mm) 4.5 i : : i 3.1 3.2 Rcession (mm) 0.0 2.0 0.5 1.1 0.9 anchoring Recession (mm) Mi i 2 2 i [ 2 2.1 barrier mem- Gain in clin. clos. (mm) 2.0 0.0 2.7 2.7 1.7 Gain in clin. clos. (mm) 0.5 0.1 0.8 0.9 0.6 before initiation of surgical Ireatmcnt. Prior to surgery, a horizontal notch was made on the facial root surface at the level o\' the gingival margin using a \ round bur. To insure reproducibility 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 distance from the gingival notch to base of clinical pocket was recorded prior to surgery and 1 week prior to block section. At the lime of surgery, and prior to root planing, a 2nd notch was made through the most apical level of visible calculus and distance from the calculus notch to the osseous crest was measured. The notching accuracy of the visible calculus was optimized in these sites, since they were at facial surfaces of anterior teeth and therefore clearly visible to the operator. Surgical procedure An intrasulcular incision was made to elevate a full.split thickness mucoperiostoal 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 lesion and root were thoroughly debrided and above described measurements recorded. At four facial sites (patient no. l)Goretex periodontal material was placed about 5 mm apical to the alveolar crest and 3 to 4 mm coronally. It was positioned to remain subgingival following suturing of the Haps. Membranes were secured with non-resorbable Goretex sutures placed circumferentially around the tooth using a sling technique. At all sites treated, flaps were then readapted without sutures and subsequently sutured coronally by anchoring the sutures to the facial orthodontic brackets (Figs. 1-5) Interrupted sutures of 4.0 silk or Dexon were utilized at all sites. No dressing was placed. Patients were instructed to rinse with Frff. 6. Overview of tooth -32 in patient no. I. HematoxyHn-eosin stain ( x 10). Note soft tissue closure within notch, and shape and position of alveolar crest. Fig. 7. Higher magnification of calculus notch shown in Fig. 6 ( x 160). Note ceniontum lining the resorbed dentinal surface and fiber attachment into cemenlum. Fig. 8. Higher magnification of crestal area from site shown in Fig. 6 ( x 25). Note resorption at the facial aspect of the labial plate, osteogenesis at the periodontal aspect o! the plate and cementogenesis at the root surface. Also note ihe tip of the crest tilting toward the root. 72 Shihl <£ Frown 1.2% ehlorhexidine gluconate twice a day for 2 weeks. Flap sutures were removed 4 weeks following surgery. Patients returned tor professional plaque removal every 2 to 3 weeks until block sectioning was performed. Block sections were removed X weeks after membrane placement in patient no. I. The non-membrane containing sites were removed in block 12 weeks after surgery to accomodate patient no. 2. At the lime of block removal, clinical records, photographs and radiographs similar lo those described at initial surgery were taken At block removal, leeth were fixed in 10% buffered formalin, decalcified in EDTA and embedded in paraffin. Step serial sections 8 /< thick were cut and stained for routine histologic evaluations using hematoxylin-eosin and trichrome stains Clinical Observations Pertinent clinical findings are summarized in Tables I. 2. Summarizing these observations, we note that average initial pocket deplh was similar in both patients. 5.3 and 5.9 mm, respectively. Average post-operative pocket depth also appeared to be similar, 2.9 and 3.2 mm. respectively. A clinical difference was seen in the average amount of gingival shrinkage recession that took place in the non-membrane containing sites (2.1 mm), while at ihe membrane treated sites, average recession was 0.9 mm. Gain in clinical closure reflected this difference, namely an average gain of 1.7 mm in the membrane treated group and 0.6 mm in the non-membrane containing sites. Obviously, the number of sites presented are too small to provide clinical data of statistical or clinical significance. Rather the aim of this report was the histologic evaluation of the healing modes which occured at the treated sites. Yet. the clinical trends noted were in synchrony with the histologic observations. Histologic Observations Membrane treated sites (patient no. 1) At 3 of the 4 sites tested, we observed "repair cementum" formation within the apical portion of the calculus notch associated with evidence of dentin resorplion. Functionally oriented fibers were found at the "'cementum" fiber interface within the notch. Incisal to the new attachment, epithelium adhered to the notched dentin as part of the junctional epithelial closure mechanism. At I of the 4 sites, the notch was epithelized. but "repair cementum" into which fibers seemed functionally inserted was seen immediately apical to the most apical border of the notch (Figs. 6, 7). Apical to the notch, we observed reformation of a stipracrestal unit. In some sections, cresta osteogenic activity was marked and the newly forming crest appeared to "bend" toward the root (Fig. 8). However, this osteogtrnic activity was not present in every serial section within a specific block (Figs. 9 II). Bone resorption at the facial aspect of the labial plate was seen in all specimens in close proximity to the membrane. At the periodontal surface of the labial plate, compensatory osteogenesis was frequently encountered. The facial root surfaces opposite the bony plate demonstrated active cem en lo genesis (Figs. 8, 11). In all specimens, the membrane was seen to be located on a thin epithelial layer which separated it from the underlying connective tissue. Inflammation was marked in the gingival margin of these specimens which reflected the significant debris accumulations seen clinically at ihe sues. The debris levels reflected the patienfs reluctance lo cleanse the operative sites. Non-membrane containing sites (patient no. 2) These sites showed plaque and calculus adhering to the dentinal wall within the calculus notch. All gingival margins were located apically to the notches and the facial attachment apparatus had shifted apically (Figs. 12. 13), No evidence of new attachment was seen at the 4 sites tested, inflammation was Fig. V. Overview of Tooth #31 in patient no. I. Hematoxylin-eosin stain ( x 10). Note soft tissue closure within notch ami shape und position of alveolar crest. Fig. 10. Higher magnification of notch urea shown in Fig. 9 ( x 160). Nolc eementum lining rcsorbed dentinal surface and fiber attachment into cementum. Fig. 11. Higher magnification of remodelling activity at the crest of site shown in Fig. 9 ( x 25). Note resorption at the facia] surface and osteogenesis at the periodontnl surface of Ihe crest. Guided tissue regeneration and coronally anchored paps 73 Fig. 12- New cementum on resorbed dcniin iit apical bonier of notch at serial section from block shown in Fig, 9 ( x l 6 0 ) . Note cemenlocyte within newl) formed cementum (arrow). present at all gingival margins in association with the marked plaque accumulations found in these locations, again reflecting the patient's reluctance to cleanse the o p e r a t i v e sitcv Comments It is generally accepted that gain in clinical closure at debrided suprabony lesions is the result of epithelial and connective adhesion to the debrided root surface (Box 1924. Levinc & Stahl 197?.. Yukna 1976. Stahl 1979, Steiner et a!. 1981). However, the GTR approach has posited that delayed epithelization of the exposed root surface may enhance new attachment at such sites. This, despite the fact, that progenitor cell presence on the root in suprabony lesions s esentially dependent on coronal upgrowth of such cells. In addition, the presence of a suprabony placed membrane could provide a physical spate necessary for the initial healing to take place by modes other than adhesion (Gottlow et al. 1986). Our current observations support such concepts, albeit in a small human sample, particularly since similar new attachment was not seen in the coronally placed, debridedonly sites. The present histologic obervations depicting new attachment at suprabony Fig. 13. Overview of tooth #31 in patient no. 2. (n on- mem bra nc containing). Hematoxylin- eosin stain ( x 10). Note plaque accumulation in notch. Apical to notch, closure occurred by junelional epithelial adhesion to the root. lesions without adjoining vertical defects appear rather consistent in these human samples. However, the degree of new attachment was limited, and variations in extent of new attachment were seen between sites and within a site. Yet. the histologic responses offer support for the concept that, biologically, supracrestal new attachment is possible in the human model. Of further interest was the accomodation responses of the labial plate to the presence of the membrane in close proximity. Compensatory facial resorption and penodonlal surface apposition were routinely observed at the labial plates of the experimental specimens at 8 weeks after membrane placement. Since healing responses including cementogenesis occur within one or two weeks after injury, (Stahl et al. 1972), it appears advisable to remove a non-resorbable membrane after the initial healing phenomena have taken place or use a membrane which will resorb within this time frame. Furthermore, it should be noted that the healing responses observed particularly at the experimental sites took place despite the marked plaque accumulations and associated ginghal inflammation. The presence of the facial orthodontic brackets and the history of recent surgery made our patients reluctant to use good oral hygiene. One can only speculate how more ideal plaque control measures would have affected the healing responses. Finally, a comment regarding the responses at the non-membrane containing sites where an apical shift of the marginal attachment apparatus took place at all sites tested. Our results are in contrast to those reported clinically by Gantes et al. (1988). However, it must be underscored that the quoted results were observed at furcation sites and followed citric acid root treatment. Thus, the morphology o\' the lesions and treatments of the root were significantly different from those present in our sample. Here again, we must recognize the influence of lesion morphology and root surface condition on gingival healing sequences. In this regard, the histologic evidence of dentinal resorption at the new attachment sites within the notches of our samples suggest the need for further study regarding the role of dentinal resorption in new attachment responses (Egelbcrg 1987. Poison 1987). Zusammenlassung Die HeUsmg von supraatveolaren Laskmat, die mil gesteuerh'r Gvweheregeneralitm hehandell wurden. Regeneration und koronal fixierie happen Fallbeispiele Bei einem Versuchspatienten wurden 4 supraalvcolare Lasionen an Unserkiefer-Frontzuhnen mit Teflonmembranen, die zwischen den Weichgewcbelappen und der Wurzel lagen, behandeh. Beim zwejten Patienten dienten 4 supraalvcolare Lasionen an Unterkiefer- Frontzahnen als Vergleich. Alle Wur/eln wurden mit UttraschaJl- und Handinslrumenten kuretticrt. Die apikalste Stelle mit Zahnstein auf der Fazialilaehe wurde mit einer Kerbe vcrsehen. Der Lappen wurde so koronal wie moglich zugenaht. wobei kieferorthopadische Brackets als Vcrankerung benut/t wurden. Die Gewebeblocke wurden 2 bis } Monate Bach dem EingrilT entfernt und die faziale Situation wurde bei alien Zahnen histologiseh untersucht. Neues Attachment in Form von neuem "Zement mit funktioneU orienticrten Fasern" wurde in 3 von 4 Zahnen. die mil Membranei! behandell wurden, innerhalb der Zahnsteinkerbe und an einem Zahn leicht apikal der Kerbe bcobachtel. Die vier Vcrglcichszahne /cigten keinerlei •Nti/eichen von neuem Attachment innerhalb oder neben der Kerbe. Der Ansatz der Gingiva war eher apikal der Kerbc gelegen. Unsere Beobachlungen lassen vcrmutcn, daB in den besehriebenen Fallen die Technik der gesteuerten Gewetvreeeneration das koronale Attachment 74 Stuhl <£ Frown bci menschlichen supraatveolaren Lasioner verbesscrte. Resume Guerison dcs lesions supra-osseuses humaines iruilces par regeneration tissulaire guid&e el lambeaux fixes sw h couronne. Comptes rendus tic cai Dcs membranes en Teflon ont cle interposccs entrc les kimbcaux dc tissu mou ct les racincs dans 4 lesions supra-osseuses humaines affeclant les incisivcs infeneurcs chez un patient volontairc. Pour la cotnparaison on a utilise 4 lesions supra-osseuses affeclant les incisivcs inferieures ehcz un aulre patient. Toutes les racines on1 etc debridees an moyen d'instruments ultrasoniqucs el manuels, et nn a marque d'unc encoche la localisation ju tartre site le plus apical sur la face vestibulaire. Les lambeaux ont etc sutures a un nivcau ausst coronaire que possible en utilisanl lies "brackets" orthodontiques pour la fixation. [)cs blocs de tissu ont etc preleves 2 a 3 mois aprcs los interventions et on a procede a 1'examcn hislologique du cote vesltbulaire dc Unites les dents. On ,i constate la presence, dans I'encoche corrcspondani au tartre pour .1 sur 4 dcs sites traites avee membrane, c( au niveau situe immediatement en apical de I'eueochepom Tun des sites, d'une nouveUe attache formce lie "cement ;i fibres onentees fonclioiinelleinenl". Dans les 4 sites servant pour In comparison, on n'observait aucun siyne mdiquant une aouvelle attache, ni dans I'encoche ni a cote d'cHe. Fin fail, les rebords gingivaux elaient situes en apical ile reneoche. Nos observations semblent indiquer que les techniques dc regeneration lissulaire guidee favorisaienl les reponses de formation d'altachc eoronaire dans les lesions supraosseuses humaines an sein de la population decrite. References Uecker, Wm.. Becker. B. H.. Prichard. J- F., Caffesse, R., Rosenberg. E. & Gian-Grasso. J. 111>S7) Root isolation for new attachment procedures. Journal of Periodontology 58, 819 X26. Box. H. K. (1924) Studies m periodontalpathology. Canadian Dental Research Foundation. Toronto. Egclbcrg, J. (1987) Regeneration and repair of periodontal tissues. Journal of Periotkmlal Research 22. Ill 242. Gantcs, B.. Garrett, S. & Rgelbcrg. J. (1988) Treatment of periodontal furcation defects (II). Bone regeneration in mandibular class II defects. Journal of Clinical Periodontology 15, 2.12 2.14. Goltlow, J., Nyman, S., Lmdhc, J.. Karring. T, & Wcmslrnm, J. (1986) New attachment formation in the human periodontium by ai.iii.leil lissuc regeneration Case repori-. Journal of Clinkai Periodontolngy 13, 604-616. Levine, L. L & Stahl. S. S. (1972) Repair follouini; pcriodontai (lap surgery with the retention of gingivnl libers. Journal of Periodontotogy 43, W 103. Nyman. S., Lindhe. J.. Karring, T. & Rylander, H. (1982) New attachment following surgical treatment of human periodonlal disease. Journal of Clinical Periodonloiogy 9. 29(1 296, Poison. A. M. (19871 Mechanisms of new attachment formation. Endodontics and Denial Traumatotogy 3, 45 57. Stahl, S. S. (1979) Repair or regeneration following periodonlal therapy. Journal of Clinical Perbdontology 6. .189-396. Stahl, S. S., Froum, S. & Tarnow, D. (1990) Human hislologic responses to guided tissue regeneration techniques in intrabony lesions. Case reports on 9 sites. Journal of Clinical Periodonloiogy 17. 191-198. Stahl. S. S.. Slavkin. H. C, Yamada, L & Levine, S. (1972) Speculation about gingival repair. Journal of Periodontoiogy 43. 395 402. Sleiner. S. S.. Crigger. M & Hgelberg. J. (1981) Connective tissue regeneration to periodontally diseased teeth (III- Hislological observation of cases following replaced llap surgery. Journal of Periodontal Research 16, 109-116. Yukna. R. A. (1976) A clinical and histologic study of healing following excisional new attachment procedures in Rhesus monkeys. Journal of Periodonloiogy 47. 701-709. Address: 5. E. Stuhl Department oj Periodonlics College of Dentistry NYU New York. NY 10010 USA