Human intrabony lesion responses to debridement, porous hydroxyapatite implants and teflon barrier membranes 7 histologic case reports* S. S. Stahl and S. Froum Department of Periodontics New York University College of Dentistry. 345 East 24th Street. New York, New York 10010. USA Sluht SS and h'roum S; Human intrabony lesion responses to debridement, porous hydroxylapatite implants and teflon harrier membranes. J Clin Periodontol 1991; 18: 61)5 -610. Abstract. 7 vertical lesions at 7 teeth in 3 adults with severe periodontitis were treated using open surgical debridemenl, porous hydroxyapalite grafts and placement of a barrier membrane. Roots were notched at both gingival margins and deepest visible calculus. Flaps were sutured coronally and patients were placed on 0.12% chlorohexidine gluconate twice daily for 2 weeks, post-surgery. Patients returned frequently for plaque control until block removal at 16 to 28 weeks post-surgery. 1 additional block was harvested after 28 weeks. The latter site received root planing only and closed by epithelial adhesion. In the 7 experimental sites, clinical responses were uneventful, and gain in clinical closure varied from 1.7 to 5.0 mm (average = 3.6 mm) Histologically, 2 sites exhibited closure by a long junctional epithelium. The remaining 5 sites showed gingival recession to be apical to the calculus notch or the calculus notch to be epithelized. However, apical to the notch and within the osseous crater, cellular cementum deposition w;is marked as was increased bone mass. The increase in bone mass was the result of osteogenesis within the surrounding graft particles which often fused with osseous seams of the crater. A functionally-oriented PDL was seen usually at these sites. Key words: intrabony lesions; hydroxyapatite implant: barrier membrane Accepted for publication 30 July 1990 In a recent position paper. Hancock (1989) staled that "combined procedures aimed at stimulating bone formation and encouraging coronal development of the connective lisssue attachment are promising approaches to regeneration". This concept is supported by Bowers et al. (I989) who concluded that "the combination of highly osteogenic materials and epithelial exclusion techniques offer promise for enhancing the amount. frequency and predictability of periodontal regeneration." Schallhorn & McClain (1988) reported on a clinical *This sludy was supposed in pan by the Claire and Melvyn Kaufman Institute for PenndonUil Research. New York University College of Dentistry. New York. New York. USA. sludy combining osseus composite grafting, root conditioning and guided tissue regeneration. They noted improved gains of vertical open probing attachments (mean gain of 5.3 mm) where the combination treatment was utilized compared to sites where membrane alone was used (mean gain 4.5 mm). On the other hand. Garret et al. (1988) using a collagen membrane, root conditioning and bone grafts at 25 intraosseous sites in 21 patients, noted unpredictable clinical results after a 1-year observation period. These observations suggested the need for human histologic evaluations of vertical defects treated with both attachment-enhancing procedures (GTR) and bone-mass-increasing materials (porous paniculate hydroxyapatite). For this report, responses in 7 sites of 3 patients will be presented. Material and Methods 7 vertical periodonta! lesions on 7 teeth in 3 adult (ages 44 to 66 years) volunteer patients (1 female. 2 male) were treated by open debridement flap procedure followed by fill of the defects using a porous paniculate hydroxyapatite (Interpore* 200). The filled defect was covered by a teflon barrier membrane (Goretex periodontal material**). All patients were in good health and each signed an informed consent following explanation of the study and providing freedom to withdraw at the patients' *lnlcrpore 2(10 is a product of Inlerpore International, Irvine. California. USA. "Goretex periodontal material is a product of W. L. Gore Associates. Inc. FlugslalT. Arizona. USA. 606 Siulil & Frown request. Surgery was performed as part of the overall periodontal treatment plan in the Department of Pcriodontics al New York University College of Dentistry. All X teetli selected were scheduled For extraction. The) had been diagnosed as hopeless, for periodontal or prosthetic reasons, by 2 pcriodontist who are not part of the present study. Prior to surgery, cause-related therapy was performed. However, root planing at the selected sites was performed only alter notching of the root ut time o\' surgery. Root dehiidcmenl was carried out using ultrasonic sealers and hand instruments until all visible calculus was removed. Hoth magnifying lenses and fiberoptic light were employed to detect calculus. All necessary pre-treatment photographs and radiograms of the sites were taken at this time and photographs were obtained during surgery for clinical documentation. In addition to the above-cited 7 sites. 1 additional block was harvested. This site (patient no. 3, tooth ••'46) was treated by debridement only and harvested at 7 months post-surgery. Measurements Prior to surgery, a horizontal notch was made at the level of the gingival margin using a 1.2 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 utilizing a number 50 silver point, a locking plier and a Holey gauge. The distance from the gingival notch to base of clinical pocket was recorded prior to surgery and I week prior to block section wherever possible. At the time of surgery, prior to root planing, a second notch was made through the most apical level of visible calculus and the following measurements were made: (I) distance from calculus notch to the deepest poinl of the osseous defect; (2) distance from calculus notch to the alveolar crest. Following defect and root debridemenl. the defect was classified according to the number of osseous walls remaining. Surgical procedure An intrasulcular incision was made to elevate a full thickness mucoperiosteal flap in order to retain as much marginal Fig. I. Clinical appearance of dehnded lesion, tooth -15, in patient Fig..?. Site al tooth -15. patient no. I with harrier membrane in place. no. 4. Fig. 2. Silo ;it tooih =1?, patient no. I rilled with Interpori graft. Fig. 4. Dehrided sile ill loolh #46, patient no. 3. This site received debridement only. Intrabony lesions treated with GTR and Imerpor e 607 gingiva as possible. After root calculus notching, the lesion and root were thorough]) debrided and above-described measurements recorded. In all sites (except in the debridement-only site), ihe vertical delect was packed to slightly above crest with the porous hydroxyapatite. Following this, the teflon membrane was placed at least 4 5 mm apical to the crest of the bony defect. It was also positioned coronally to remain subgingival following flap suture. Membranes were secured with nonresorbable sutures placed circumferentially around the tooth using a sling technique. The flaps were readopied without sutures to allow adjustment of the position of the membranes and then sutured coronally in these positions with interrupted sutures of 4-0 silk or Dcxon. No dressing was placed. Patients were instructed to rinse with 0.12",, chlorohexidine gluconate 2x a day for 2 weeks. Flap sutures were removed 10 14 days following surgery. Patients returned for plaque removal once a week for 1 month, then every 2 to 3 weeks until hlock section was performed. Teflon membranes harrier were removed 6 to 8 weeks after placement during a 2nd surgical procedure. Block seclions were removed 16 to 2* weeks after surgical therapy. At the time of block removal, clinical records, measurements, photographs and radiographs similar to those described at initial surgery were taken (figs. 1-3). Histologic processing and measurements At the time of 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 routine histologic evaluations. The length of new cementum was measured microscopically in 3 centralK located step serial sections (61) ft Fig. 5. Histologic overview of site shown in Fig. 4. H&E slain. Note calculus notch is epithclizcd and closure is by long junttionul epithelium. apart). They were measured in a linear direction alone the root surface. The new cementum was measured from its most coronal to its most apical root position, but never beyond the base of the osseous crater. The distances reported per site are the mean of 3 measurements taken per block (Table 1). Observations Clinical Pertinent clinical findings at each site are presented in Table 1. In summary, the clinical findings for sites removed 16 to 28 weeks after surgery showed an average preoperative pocket depth of 9.5 mm (range 7.5-13.0 mm) and a postoperative average pocket depth of 4.S mm (range 2.8-8.2 mm). Recession averaged 1.4 mm (range 1.0-1.7 mm) and gain in clinical closure averaged 3.6 mm (range 1.7 5.0 mm). Fig. 6. Histologic overview of site shown in Fig. I. This site received the lnterpore graft and barrier membrane and the block was harvested 16 weeks after surgery. H & E stain. Noleepithelized calculus notch. Apical lo the notch, cellular cementum is present which contains inserlcd fibers emending into She connective tissue surrounding Ihe graft particles. For the debrided-only site, (patient no. 3, tooth ^46) the clinical measurements were as follows: preoperative pocket depth =12.2 mm, postoperative pocket depth = 7.0 mm. recession = 3.6 mm and gain in clinical closure = 0.8 mm. The observation period was 28 weeks. No unusual sequelae were noted for any patient during the entire period of observation and healing progressed satisfactorily at all sites treated. Histologic Debrided-only site The histologic findings at this site demonstrated closure by epithelial adhesion (long junctional epithelium). The calcu- I'tibic I. Responses following use of debndement. hydro.xyapatitc tirufl and barrier membrane Patienl no. 1 : 333 33 I'D nockel Tooth 25 52 16 17 ! s 36 depth. Initial P.D. (mm) - II 13.0 9.8 8.7 10.1 9.5 Observation time (weeks) 16 16 28 > 2S 28 28 Posl-surg. P.I). (mm) 2.8 8.2 6.8 3.0 4 II "Mi Recession (mm) .6 0 .3 .7 0 .5 .5 Gain in clinical closure (mm) 3.6 3.8 1.7 B 4.7 4.6 5.0 New cementum (mm! 2.4 1.4 1.0 IMI 0.9 1.1 0.0 608 Stah! & Froum Fig. 7. Higher magnification (25 x ) of cellular ccmcnlum shown in Pig. 6. lus notch was lined with epithelium and the vertical osseous seam showed no evii l c l l L V o l x l L J I I l i k M l l l < . s k . i ; v l l r - l , ( I \i'\ 4, 5). Membrane and hydroxyapatite treated site; 16 in 28 weeks post-surgery Of the 7 sites harvested, 2 sites exhibited closure by epithelial adhesion (long junctionat epithelium) and demon si rated no evidence of osteogenesis or new attachment. The remaining 5 sites showed epithelial lining wilhin the calculus notch or gingival marginal recession to root sites apical to the calculus notch. However, at these apical root sites and within the osseous crater, cement ope nesis was often Fig. 9. Histologic overview of site shown in Fig. K. H & E stain. Note cellular cementum apical to calculus notch and adjacent lo ossifying graft particles. pronounced along the root surface. It was coupled with notable osteogenic activity within and at the borders of the graft particles which frequently appeared fused to the alveolar walls and crest (Figs. 6 10), The periodontal membranes appeared well organized in most sections examined. Length of new cellular cementum measured coronally-apieally along the root surface averaged 0.9 mm and ranged from 0.00 mm to 2.4 mm (Table I). It should be noted that osteogenesis within and surrounding graft particles was seen at some locations directly opposite the long junctional epithelium Fig. 8. Clinical appearance ofdchrided site of tooth «37 in patient no. 3. This site was treated wiih Interpore graft and barrier membrane and the block was harvested 28 weeks after surgery. Fig. 10. Higher magnification of site shown in Fig. 9. Magnification 64 x . Note character of cellular cementum and osteogenic activity within graft particles. (Fig. 11). Thus, graft osteogenesis did not correlate directly with cemenlogenesis in our samples. Nor did clinical probing changes (gain in clinical closure) indicate the histologic nature of the closure. Tn fact, the site showing the largest gain in clinical closure (5.0 mm) demonstrated historically a long junctional epithelium without any evidence of regeneration. Comment The question raised in the introduction, namely does a combination of a barrier membrane and a porous hydroxyapatite increase new attachment in human vertical lesions, cannot be answered positively on the basis of the case reports presented. Rather, the present responses, in some aspects, appear similar to our observations in human intrabony lesions where barrier membranes only were used (Stahl et ai. 1990). For example, cetnental deposition measured in a linear direction on treated roots in those sites ranged from 0.5 to 1.7 mm. a range very similar to that reported in the present cases. On the other hand, bone mass appeared more pronounced with the use of hydroxyapatile graft material. Obviously, our site numbers are too smalt for statistical evaluation. However, the trends seen in our clinical responses are similar to a published clinical study in which grafting, root conditioning and GTR were used (Schallhorn& McClain 1988). Intrabony lesions treated with G TR and Interpore 609 Fit;. II. Histologic overview of treated site .it tooth (136 in patient no. 3. The site was Heated with lntcrpore graft and barrier membrane and the block harvested 2S weeks after surgery. H & E stain. Note closure by long junctional epithelium and ossification in adjacent graft particles. Regarding histologic evidence of new attachment, the data presented heie must be compared with published histologie observations of increased new attachment when barrier membranes and root debridement were used (Nyman el al. 1982, Gottlow et al. 1986. Stall I el al. 1990). It should be noted that c.-- mentogenesis with functional fiber attachment did not lake place within the calculus notches of the present sites, but rather apical to the notches. Thus, the possibility must be considered that the apical eementogenesis may depict leattachment rather than new attachment. Our present observations confirm published human histologic observations of increased bone mass when porous hydroxyapatite particles were placed in vertical lesions. However, cementogencsis was no/observed when this graft material tilow was used. (Stahl & Froum 1987). Therefore, the combination utilized in the present cases appeared to enhance cementogenesisand increase hone muss within the limits of lie osseous crater. (In this context, it is of interest thai in a clinical study, Bowen et al. (1989) reported similar bone fill when porous hydroxyapalile grafts or osseous allografts were used in human vertical lesions). Finally, in comparing our results with published data, we concur with Gottlow et al. (1986) that "the amount of new attachment vanes with specific sites Vi hen the GTR technique is employed". Among the reasons for such variations. Gottlow et al. (1986) speculated that "in the presence of an angular bony defect, a space exists between the osseous walls and the root into which bone-forming cells in the periphery of the defect can migrate". Indeed, the maintenance of such vertical space using porous hydroxyapatite grafts was associated with notable osieogenesis and cementogenesis within such spaces in 5 out of 7 sites we examined. However, il did not enhance new supracrestal attachment (Nyman & Karring, 1979). In turn, lack of marked supracrestal attachment may relate to the positioning of the flap margin, since coronal anchoring of the gingival margin enhanced supracrestal new attachment in human supracrestal lesions treated by the use of debridement and a barrier membrane (Stahl & Froum 1991). A final comment: our debrided-only block was used for guidance of responses, since il was taken from a patient who also received the combination treatments at other sites. The epithelial closure observed at the debrided-only site supports published observations of this mode of closure following root debridement alone (Hancock 1989). Zusammenfassung Die Heitung vonmervxklichen Knochentaschen nach: BetageMfemtmg, Implantation pordsen Hydroxylapatits und Teflon- Membran- Einbringung. 7 histologische Fallbeispielc Bei S erwachsenen Versuchspersoncn mil schwerer Parodontitis wurden an 7 Zahnen 7 vertikalc Knochendefekle durch eine ofl'ene chnuivischc Fkl.iiiL-iHl'muinu. Implantation porcisen Hydroxylapatils und Einbringung von Membranen behancleh. Die Wurzeln wurden sowohl an der marginalen Gingiva, als aueh an tier tiefsten Slelle mil sichtbarem Zahnstein eingekerbt. Der Lappen wurde korona! angenaht Nach der Chirurgie spiilten die Patienlen zwei Wochen lang zweimal ta'glich mit 0.12% Chlorhexidin-Diglukonal. Von der I6len bis 28ten Woche kamen die Patienten ha'ufig zur Plaquekontrolle. Bis zur Blocksektion n.ieh 16 his 2X Woehen kamen die Patienten hiiufig zur Plaqueentfemung. Ein zusatzlicher Block wurde nach 2X Wochen entnomnien. Die letziere Stelle erhiell nur cine Wurrelglatlung und heilte durch epithehule Adhasion. Uei den 7 experimenteUen Defekten war die klinische Heilung ohue hesondere Vnrkommnisse und der Gewinn an klinisehem Attachment variicrte von 1.7 bis 5.0 mm (Durchschnitl = 3.6 mm) Histok)- gisch zeigten 2 Stelleti einen Verschluli durch ein langes Saumepithel. Die \erbliebenen 5 Sldleil vviesen Oingivarezcssionen bis apikal der Kcrbe auf oder hatten eine epithelialisierte Zahnsteinkerbe. Jedoch befand sich apikal der Kerbe unii innerhalbdes Knochenkraters eine Abiagerung zelluliircn Zementes und cine groliere Knochenaafl'iillung. Die Vermehrune des Knochens war das Ergebnis einer Osteogenesf innerhalb und in der Umgehuii!; der Implantatpartikel. die oft eine Fusion mil den knoehernen Begrenzungen des Kralers zeigten. Ein lunklionell orientierles parodontates Ligament wurdegewohnlich an diesen Stellen gesehen. Resume Reactions tks Itsions intra-osseuses kumaines uu traitement pur debridement, implants p<>- reux d'hydroxyapatite el membranes burr tens, de teflon. Rapports histolitgiques sur 7 eta Chez 3 adultes, alleints dc parodonlite severe, 7 lesions verticales sur 7 dents onl lite traitees en utilisant un debridement chirurgical a ciel ouvert. des greffcns poretn d'hydroxyapatile et interposition d'une membrane comme harriere, Des encoches onl ete pratiquees sur les radnes au nheuu du rebord gingival et au nivcau le plus profond du tartrc visible. Les lumbeaux ont ete sutures au mvean des couronncs et on a prestrit aux p;ilients des rincages au gluconale de ehlorhexidinea 0.12%. 2 fois par jour pendant 2scmaines apres l'inlervention. Les patients recevaient des seances frequentes de eonlrole de la plaque, jusqu'a ce i[ue soit fait un prelevement en blot 16 a 2K semaines apres I'inlervention ehirurgicale. Un bloc suppleinenlaire a ete preleve apres 2S semaines, Dans le site LIL1 ce bloc, seul un sui lat;age raiiiculaire avail tie fail, el la lermelure selail I'aile par adhesion epilheliale. Dans les 7 sites experimentaux, les reactions cliniques avaienl ele sans complications, le jiain de la cicatrisation clinique variait de 1.7 a 5.0 mm lmoyenne = 3.6 610 Siahl <£ Frown mini. A I'examen histoiogjque, _ des silcs avaicnt unecicatrisation avec long epithelium dc jonetion. Les 5 autres sites presentaient uno recession gingivale en apical de I'encoche, on une epilhelialisation de Pcncoche faite au niveau due tarire. Cependant, en apical de rencocfae el a I'interieur du cratere osseux, il s'elait produil un depot marque de cement colluliiirc. ainsi iju'iinc nette agumentatioti de la masse osseuse. Cette augmentation de la masse osseuse emit le resultai de t'osteogenese se produisanl dans les particules dcs grelfons et autour d'elles et entrant s.mvenl en fusion avec les hords osseux du cratere. Un desmmlonlc oriente suivant la fonclion etatt gcncralcmcnt constate dans ces sites. References Bowen, J. A.. Mellonig. J. T.. Gray, J. L. & Towle, H. T. (I9S9| comparison of decalcified I'ree/e-dried bone allografl and porous paniculate hydroxyapatite in human periodonta! osseous defects. Journal of Periodontology 60. 647-654. Bowers. G. R. et al. U9N9] Histotogic evaluation of new attachment apparatus fbrmafytion in humans, part li. Journal of Periodontology 60, 675-682. Garret. S.. Loos, B.. Chamberlain. D & I gelberg, J. (1988) Treatment of intraosseous periodonlal defects with a combined therapy of citric acid conditioning, bone grafting and placemen! of collagenous membranes. Journal of Clinical Periodontology 15, 38J-389, Gotliow. J.. Nyman. S . Lindhe, J.. Karring, T. &Wern strom, J. (1986) New at Inch men I formation in the human periodontium b\ guided tissue regeneration. Case reports. Journal of Clinical Periodontology 13, 604-616. Hancock. H. B. (1989) Regeneration procedures. In: Proceedings of the World Workshop on Cliniuil Pcrioilomtcx. The American Academy of Periodontology, pp 11-13. Nyman, S. & Karring. T. (1979) Regeneration of surgically removed buccal alveolar bone in dogs. Journal of Periodonlal Research 14. 86-92. Nyman, S., Lindhe, J., Karring, T. & Rylandcr. H. (1982). New attachment following surgical treatment of human periodonta] disease. Journal of Clinical Periodontology 9. 290-296. Schallhorn. R. G. & McClain. P. K. (1988) Combmcti osseous composite grafting, root conditioning and guided tissue regeneration. International Journal oj Periodontics ami Restorative Dentistry 4. 9-31. Stahl, S. S. & Froum. S, J. (1987) Hislologic and clinical responses to porous hydroKylapatite implants in human periodonlal defects. 3 to 12 months posiimplantalion. Journal of Periodonlology 58. 6S9 (>95. Stahl. S. S.. Froum, S. J. & Tarnow. I). (1940) Human EiisloEogic responses to guided tissue regeneration techniques in intrabony lesions. Case reports on 9 sues. Journal of Clinical Periodontology 17. [91 198. Stahl, S- S. k Froum. S. 3 (1991) Mealing of human suprabonj lesions treated with guided tissue regeneration and coronalK anchored Haps, Case reports. Journal of Clinical Periodontology 18. in press. Address; S. S. Slah! Department of Ptriodontics New York University College oj Dentistry }4i East 24th Street New York, N Y 10010 USA