Healing Responses of Human Intraosseous Lesions Following the Use of Debridement, Grafting and Citric Acid Root Treatment

II. Clinical and Histologic Observations: One Year Postsurgery*

S. Sigmund Stahl, S. J. Froum and L. Kushner

Accepted for publication 26 October 1982

Recently we described human histologic healing responses following the treatment of intrabony lesions using open debridement and a variety of augmenting procedures. For those papers, we reviewed the pertinent literature and described the therapeutic and evaluating procedures in detail.1-3 In these publications, we described 6-month postsurgery healing responses. Following similar therapy and evaluation, the present paper reports on healing responses observed both clinically and histologically 12 months postsurgery. We again placed notches through calculus accretions at different levels of involved root walls prior to root planing in order to further test the hypothesis that attachment "regeneration" depends on its proximity to vital ligament tissue. In combining these findings with previously reported short term healing responses, we hoped to more completely circumscribe human periodontal healing following a variety of therapeutic measures used in treating intraosseous lesions.

MATERIALS AND METHODS

Two patients were selected from those present for periodontal diagnosis and treatment at the dental clinic at the Veterans Administration Medical Center, New York City. Because of some variation in medical history, initial therapy and method of documentation, these cases will be described separately.

Measurements

A previous paper reporting on three block sections described the initial treatment prior to surgery and the method of measurement.3 As in that study, all present measurements were again recorded to the nearest 0.1 mm prior to initial surgery and 2 weeks prior to block section using a grooved, custom-made omnivac acrylic stent, a boley gauge, an endodontic silver point and locking pliers (Tables 1 and 2).

*A.G., autogenous bone graft; O.A.. citric acid.

Figure 1. Preoperative clinical photograph of maxillary left central and lateral incisor showing probe in position.

Description of Sample

Patient I.  A 24-year-old male had an unremarkable medical history except for an allergy to penicillin. Clinical and radiographic examinations revealed advanced periodontal disease around all the maxillary teeth. Moreover, for both periodontal and prosthetic reasons full arch extractions were indicated followed by construction of a full denture. The patient agreed to participate in a study which included performance of various surgical procedures at different time intervals prior to extraction.

Figure 2. Preoperative clinical photograph of maxillary right canine with probe indicating clinical pocket depth.

The nature of the surgical procedures and selective block section extractions were explained to the patient and written consent was obtained prior to each surgical procedure.  Presurgical treatment consisted of oral hygiene instruction, supragingival scaling and occlusal adjustment for gross occlusal interferences. Every attempt was made not to remove subgingival calculus during scaling. Prior to surgery, clinical measurements, photographs and radiographs were obtained (Figs. I and 2). Immediately before surgery, the mesial root of the right canine and distal root of the left central incisor teeth were notched with a No. 1/2 round bur at or slightly below the level of the gingival margin. The surgical procedures performed simultaneously at both teeth consisted of an inverse bevel incision and reflection of a full thickness mucoperiosteal flap retaining as much of the marginal gingiva as possible. Upon exposure of the roots and the canine and central incisor root surfaces were again notched through the most apical extent of existing subgingival calculus into dentin.

Figure 3. Debrided lesion at maxillary left central and lateral incisors.

Figure 4. Debrided lesion at maxillary right canine. Defect.

In addition, the mesial root surface of the left lateral incisor was notched at its most apical calculus deposit. The calculus and deposits were then removed from all teeth. The defects were debrided, irrigated with isotonic saline, measured and photographed (Figs. 3 and 4). Prior to implantation of the graft materials, intramarrow penetration of the defect walls was performed with a No. 23 explorer in order to conform with the protocol of the previous study. The one-wall intraosseous defect on the mesial of the right canine was overfilled with durapatite* graft material (40-60 mesh) (Fig. 5). The two-wall intraosseous defect on the distal of the left central incisor tooth was overfilled with decalcified freeze-dried allogenic bone obtained from the U.S. Navy bone bank (Fig. 6). The flaps were coapted and sutured at or close to the presurgical gingival level with interrupted 4-0 silk sutures. An attempt was made to obtain maximum interproximal coverage. A Coe-pak dressing was applied to the area. Following the surgery the patient was placed on erythromycin. 1 gm/ day for 10 days. He returned 10 days postsurgery for suture removal and then every 2 weeks for 2 months. At each of these visits it was noted that the patient's home care was very poor. Each postsurgical visit included a review of oral hygiene instruction and debridement of the treated sites. Unfortunately, contact was lost with the patient for the next 6 months during which time he was treated on an out-patient basis for alcoholism. Ten months postgraft surgery the patient returned to continue his dental treatment. His gingiva was severely inflamed and heavy plaque and calculus deposits were present. Over the next 6 weeks multiple scalings and root planings. together with improved home care, decreased gingival inflammation. Two weeks prior to extraction, pocket depth measurements were again recorded and radiographs of the graft sites were taken (Figs. 7 and 8). Probing revealed that the pocket depth on the mesial of tooth No. 6 had decreased from a preoperative measurement of 6.1 mm to the current 2.1 mm.  

Figure 5. Lesion at right canine with durapatite graft in place.

* Durapatite is a high density, high purity form of hydroxylapalite marketed by Cook-Waite Laboratories. Inc. as Periograf™

Figure 6. Lesion at left maxillary Incisor with allograft in place.

Figure 7. Radiogram of maxillary right canine 12 months postsurgery. Arrows point to notches.

Figure 8. Radiogram of maxillary left central and lateral incisors 12 months postsurgery.  Arrows point to notches.

The pocket depth on distal tooth No. 9 showed a decrease from a preoperative measurement of 7.1 mm to the current 2.8 mm. Twelve months postsurgery, both teeth were removed in block section (Figs. 9 and 10). An immediate full denture was inserted and the areas healed uneventfully.

Histologic Observations: Mesial Root Surface of Maxillary Right Canine

A histologic overview of the specimen is shown in Figure 11. At this low magnification, the position of the two notches and their relation to the adjacent alveolar crest is evident. A higher magnification of the site indicates that the notch placed at or slightly below the gingival margin is lined with epithelium which becomes a junctional epithelium apical along the root surface until it reaches the incisal border of the more apically positioned notch (placed at the most apical extent of calculus) (Fig. 12). The connective tissue located within the osseous lesion at the more apical notch does not appear functionally organized, nor is there histological evidence of cementogenesis within the notch. Yet, the connective tissue shows no evidence of an inflammatory infiltrate and thus could best be described as a "fill." in close proximity to the alveolar wall.  

Figure 9. Postoperative appearance of surgical site at maxillary right canine 12 months post surgery.

Figure 10. Postoperative appearance of surgical site at maxillary left incisors 12 months postsurgery.  

Figure 11. Overview of histologic specimen, mesial No. 6. Arrows point to the notches.

Figure 12. Notched root surface of mesial No. 6.  Note the incisally placed notch is lined by epithelium. Junctional epithelium adheres to the root surface immediately below the notch and is limited by connective tissue piling the more apically positioned notch (magnification x 25, H & E.

Figure 13. A higher magnification (X 25) of the more apical notch within the osseous lesion shows connective tissue filling the notch. However, no evidence of cementogenesis is seen. Note also, empty spaces within the "fill" denoting previous presence of durapalite particles.

Within this "fill," empty spaces indicate durapatite particles were present (Fig. 13). The borders of the durapatite particles consist of connective tissue without evidence of osteogenesis at the particle seams. No inflammatory infiltrate is present in this area. Thus, as suggested previously.2 the graft particles appear to be well encapsulated, noninflammatory producing and acting as a filler within the connective tissue repairing this lesion (Figs. 14 and 15). Root Surfaces at Maxillary Left Incisors The specimen shows varying repair responses within the confines of the lesion (Figs. 16 and 17). It should be remembered that this lesion was in a patient whose oral hygiene was poor; thus, presence of significant gingival inflammation is not surprising. The lesion had been filled using an allograft. Despite the placement of this graft 1 year prior to extraction, exfoliation of spicules is still evident throughout the specimen (Fig. 18). Of particular interest at this level of the section is the repocketing seen at the level of the incisal notch (placed at about the height of gingival margin). The lining epithelium becomes junctional epithelium at the level of the more apically positioned notch. Within this notch, however, cementogenesis and functionally attached fibers are seen at its most apical border (Fig. 19).

Figure 14. Photomicrograph of area immediately apical to notch shown in Figure 13. Note well encapsulated border of decalcified durapatite panicle (magnification x 64)

Figure 15. Higher magnification (X 100) of seam of decalcified durapatite particle showing no evidence of osteogenesis at its seam.

It should also be noted that some of the graft spicules show limited evidence of osteogenesis at their seams (Fig. 20). A more centrally located serial section of the block (Fig. 16) presents further evidence of graft spicule retention 1 year after surgery. The distal surface of tooth No. 9, in this area, has the incisal notch lined by epithelium. This epithelium changes to a long junctional epithelium which is limited apically to the level of inserted fibers (Fig, 21). These sections, therefore, again demonstrate gradations in healing responses varying from repair to "regeneration" of lost attachment within the same lesion. 1,3 Thus, epithelial adhesion and new attachment may both be present at similar root levels, albeit not in the same level of a section. In this section (Fig. 16) we also see the notch site at the mesial of tooth No. 10. Here, the notch had been placed at about the most apical level of calculus, well within the confines of the adjacent osseous wall. In this area, we encounter limited apical migration of the junctional epithelium and evidence of cementogenesis with fiber insertion immediately below the epithelial adhesion (Figs. 22-24). It should be emphasized that this new attachment is in close proximity to the base of the lesion; thus, viable periodontal ligament cells may well have constituted a "donor" source for this new attachment.

Figure 16. Overview of the specimen consisting of the maxillary right central and lateral incisors.

Figure 17. A serial section of specimens shown in Figure 16 demonstrating the two notches on the mesial wall of the central incisor.

Figure 18. A higher magnification tx 10) of mesial wall of No. 9 shown in Figure 17. This site shows inflammation and sequestration of graft spicules.

Description of Sample

Patient II.   A 45-year-old male revealed a medical history of rheumatic fever and arthritis. Medical clearance was obtained and on his physician's instructions the patient was premedicated with penicillin prior to all periodontal treatment, according to the recommendations of the American Heart Association.

Figure 19. A higher magnification of apical notch area at distal No. 9 (X 64) showing cementogenesis and fiber insertion at the most apical portion of the notch (arrow).

Figure 20. Within the area shown in Figure 19, note evidence of osieogenesis (arrow) around some graft spicules (magnification X 64).

Figure 21. Higher magnification x 25} of section shown in Figure 16. Note long junctional epithelium apical to incisal notch. The more apically located second notch is facially located to this plane of section and thus does not appear.

His dental history included having been treated for periodontal disease at the New York Veterans Administration Hospital in July 1974 by initial root planing followed by surgical pocket reduction utilizing apically positioned flap surgery and osseous reshaping in the lower incisor and cuspid teeth. The patient was re-examined 2 years later (March 1977) at which time the anterior teeth showed recession, severe osseous loss and repocketing of from 5.3 to 10.2 mm. Mobility of these teeth was recorded as Class II and III and the teeth were given a hopeless prognosis. With the patient's consent, it was decided to treat the teeth prior to block extraction. Treatment included construction of a wire and composite splint with No. 23-24 splinted with wire and these and the remaining teeth splinted with an acid-etch composite. Appropriate presurgical treatment and measurements were performed as described above (Figs. 25 and 26). Periodontal surgery was performed on March 15, 1977 consisting of reflection of an inverse bevel full thickness mucoperiosteal flap, debridement of the defects and root accretions and implantation of an autogenous osseous coagulum-bone blend graft (Figs. 27 and 28). The donor site consisted of the edentulous areas in the maxillary arch including the tuberosities. Both cortical and cancellous bone were utilized as the implant material. Prior to implantation of the graft in the distal No. 25, mesial No. 26 and distal No. 26 sites, citric acid (pH = 1) was applied to the root surfaces for 4 minutes, changing the applicator every 30 seconds. To ensure exact placement of the acid, a prefabricated rubber dam was inserted around the incisors at the level of the alveolar crest.

Figure 22. Higher magnification of notch at mesial No, 10 shown in Figure 16 (magnification X 25).

Figure 23. The tooth-soft tissue interface immediately- below the epithelium in the area shown in Figure 22 (magnification X 64). Note cementogenesis within notch (arrow) and evidence of fiber insertion into this cementum.

Figure 24.  A more apical area of notch site shown in Figure 23 /magnification X 64). Note evidence of lacunor spaces in the new "repair" cementum (arrow) and evidence of fiber insertion.

Figure 25. Preoperative clinical photograph of site in Patient II.

The remaining sites (No. 23 mesial and distal, No. 24 mesial and distal and No. 25 mesial) were implanted after debridement and irrigated with saline for 4 minutes (similar to the application of the citric acid). Closure was by means of interrupted sutures of 4-0 silk. The sutures were removed 1 week postoperatively and the area was debrided. The patient was then seen once a month for the next 13 months. At each visit teeth No. 22 to 27 were scaled and polished, and oral hygiene procedures reinforced. Two weeks prior to block section, radiographs and clinical probings were taken of each site (Figs. 29 and 30)

Figure 26. Preoperative radiogram of site in Patient II Figure 27. Operative site debrided in Patient II.

Figure 28. Autograft in position at surgical site in Patient 11.

Figure 29. Postoperative appearance of surgical site in Patient II 13 months after surgery.

Figure 30. Postoperative radiographic appearance of surgical site in Patient II 13 months after surgery.

(Table II)- Thirteen months postsurgically, a block section was removed from teeth No. 23 to 26, including the surrounding bone and gingiva. To ensure as little postoperative deformity as possible, a free palatal soft tissue graft was transplanted to the area where the section was removed at the time of the surgery. Healing was uneventful and resulted in little or no deformity.

Histologic Observations: Lower Incisor Teeth

At this site, healing is evident in the form of elongated junctional epithelial adhesions, crestal remodelling and limited supracrestal cementogenesis into which fibers are functionally inserted (Figs. 31-33). These responses are similar to those seen at the citric acid-treated root sites (Figs. 34—37). Here again, we observe limited coronal "regeneration" of new attachment spatially seen at sites exceedingly close to the crest and periodontal ligament. Although no notches were placed in these teeth, comparison of the healing phenomenon taking place at these sites suggests again that attachment "regeneration" may depend spatially on its proximity to viable existing attachment. This healing sequence, in our samples, occurs regardless of augmenting procedures used in the treatment of intraosseous lesions. Unfortunately, our limited sample does not allow accurate comparisons of the degree of this "regenerative" response. However, autogenous grafts appear to enhance the "regeneration" potential most effectively, and in our sections, maturation of the healing process appeared most mature in sites in which autogenous grafts were used. However, it must be stressed that similar responses have been observed without augmenting procedures.33 In summary, the specimens presented demonstrate clearly that "new attachment" can take place at root surfaces previously covered with calculus. However, this regenerative phenomenon seems closely related to its proximity lo viable cells from the existing periodontal ligament. The latter, in turn, may well act as a "donor site" for cells capable of inducing cementogenesis, osteogenesis and a functioning ligament at a new attachment site.

Figure 31. Low magnification of mesial No. 23 (x 25). Note long junctional epithelium limited apically by inserted fibers.

Figure 32. A higher magnification of area apical to the junctional epithelium shown in figure 31 (x 64) indicates cementogenesis at the root surface with functional fiber insertion at this site. The spacing between fibers is a preparation artifact.

Figure 33. This photomicrograph of the osseous crest seen in Figure 31 shows significant osseous remodeling with limited crestal regeneration (magnification X 64).

Figure 34. Low magnification of root surface at distal No. 26 (magnification X 25). This surface had been treated with citric acid prior to autogenous graft placement.

DISCUSSION

Augmenting procedures in periodontal therapy have been documented extensively using both experimental and human models.1-15   Since a recent evaluation of artificially created periodontal defects again points to the potential problems in comparing responses of such lesions to the human lesions,16 the present discussion will draw primarily on published human data. While reported therapeutic techniques and evaluation methodology vary widely, the conclusion can be drawn that within a relatively short (approximately 6 months) post-therapy evaluation period, clinical and histologic findings document the occurrence of new connective tissue attachment to root surfaces previously exposed to the oral environment. Such results have been reported following debridement alone and debridement plus augmenting procedures. Significant controversy, however, exists when one attempts to define "the most predictable and most favorable treatment approach" to obtain regeneration. Long term histologic case evaluations17-18 have demonstrated that new attachment is maintained for at least 5 years post-therapy, that graft spicules are present for this length of time and that remodeling of osseous and cemental structure plus an organized, functional periodontal ligament are taking place in such specimens. The above cited studies certainly support our findings. Thus our material merely adds to the general body of histologically documented healing responses in human intrabony lesions. However, we believe that our observations suggest further definition of the healing process. As reported recently, we3 like Cole et al.14 notched the root at root sites covered with calculus prior to debridement and other therapeutic sequences, with the notch serving as a marker for a new attachment site. Published observations demonstrate new attachment (i.e.. cementogenesis, osteogenesis and a functionally oriented ligament) histologically especially in the area of notch.

Figure 35. A higher magnification of graft exfoliation shown in Figure 34 (magnification X 64).

Figure 36. Area at crest of specimen shown in Figure 34. Note crestal remodeling with limited evidence of crestal osteogenesis. Immediately incisal to this is new cementum at the root into which oriented fibers insert (magnification X 64).

Figure 37. A higher magnification of the area of cementogenesis (magnification X 100) shown in Figure 36. Note the oriented fibers inserted into cementoid (arrow).

This healing response may be related to spatial configuration of a notch as suggested by Morris.19 However, if one looks at our present specimens and those published previously,3 it becomes apparent that the distance between the notch and functioning periodontal ligament may well determine whether the repair process takes the form of a long epithelial adhesion or new attachment. For example, let us look at Figure 16. Here, we note that repair at the notch in the distal surface of the central incisor which is located more coronally than the notch at the mesial surface of the lateral incisor showed healing by adhesion with no evidence of new attachment. At the same interdental site, the notch site at the lateral incisor which was placed in close proximity to the existing periodontal ligament demonstrated significant remodeling and new attachment. This response, although to a limited extent, was also seen at the more apical notch at distal No. 9 despite the marked inflammation present at this site. The distance between notch and existing ligament and alveolar crest was within a 2 mm limit. Similarly, the more apical notch site of the treated lesion (Fig. 11) showed connective tissue closure, while the more incisal notch site at the same tooth surface demonstrated an epithelial/root interface. If we now turn to published reports which provide data of gain in attachment in millimeters, they indicate a range of 1.2 to 3.4 mm of gain with a clustering around 2 to 3 mm. Such coronal attachment gains did not depend on a specific therapeutic procedure.1-15  In this connection, it is of interest to note that free gingival grafts also survive best when they are no wider than 2 to 3 mm.2, 20, 21 Survival of free grafts obviously depends initially on nutrient diffusion from surrounding tissues and biologically determined distances from the recipient-bed cannot be exceeded if viability of the soft tissue graft is to be predictable. Similarly, zero depth pockets created by gingivectomy in humans show a marginal coronal gain of 1 to 2 mm 12 weeks after surgery.22 Here too, the gingival/periodontal connective tissue wound base must, of necessity, serve as the "donor site" for the marginal regeneration of the new gingival unit, and similar spatial limitations as in grafts seem to be operative. Conceptually then, we may assume that similar biological spatial limitations (proximity to periodontal ligament) govern new attachment in the healing of intrabony lesions. Supporting this hypothesis are animal and in vitro studies indicating that viable periodontal ligament cells are necessary for new attachment and that their proximity to the newly forming attachment is crucial.23,24 In this vein, it should also be noted that experimentally, new connective tissue attachment to root may occur when vital pulpal cells encounter a healing gingival wound at the tooth/soft tissue wound site. This new attachment takes place only when viable pulpal cells are present which lay down repair dentin at the site of injury.25-28 Thus, this experimental model further supports the concept that viable cell lines capable of producing a calcifying root surface appear necessary for new attachment. Such cell lines seem to be present in both pulp and periodontal ligament. Obviously, in clinical practice, periodontal ligament cells become the only reasonable cell source for new attachment. And as pointed out by Garett et al.23 in an experimental model, "the location of the notches near the apical extent of the lesions, and close to the periodontal ligament, may explain the predilection of new cementum formation." Utilizing this concept, we can explain variations in closure within an intrabony lesion (i.e., adhesion, new attachment and gingival recession) following therapy.29 Clinical evaluation of new intraosseous lesions routinely shows variations in configurations within the same lesion, thereby creating different spatial configurations with regard to the location of viable crestal periodontal ligament cells. If we speculate further, this principle may govern higher rates of new attachment in narrow three-wall lesions than found after treatment of one-wall lesions. A three-dimensional visualization of a narrow mouthed, three-wall lesion demonstrates close proximity of the attachment apparatus to the lesion at its entire periphery. This, in turn, may be a key factor in obtaining new attachment. Obviously, such proximity is not present in the same spatial orientation in intraosseous defects with less than three walls. By contrast, long epithelial adhesion closure, usually seen in healing responses following coronally placed flap procedures, is based on epithelial closure of an open wound which is fundamental to normal healing and on epithelization of the connective tissue of the soft tissue flap with its ultimate adhesion to the root coronal to an inserted fiber attachment.30 If indeed, the root surfaces can accept epithelial adhesion, a long junctional epithelium results. If not, repocketing takes place.31-35 In the normal healing sequence of any intraosseous lesion, various combinations of all three (new attachment, epithelial adhesion and repocketing) forms of repair/ regeneration probably occur.33-36 However, new attachment may be biologically limited to close proximity of viable "donor cells" from the periodontal ligament.37 The present data supports our short term results in which similar healing sequences were noted.3 It is important to emphasize that this regulating mechanism was seen with the use of debridement alone and augmentation such as autogenous osseous grafts as well as allografts. It thus seems to be the crucial determinant in creating an environment capable of "regeneration" of lost periodontal attachment. The healing in older specimens, in which autogenous grafts were used, appear more mature than that seen with allografts. However, the smallness of the allograft sample size does not allow for any definitive histologic conclusion regarding the enhancement of new attachment by this graft material. The continued presence of graft particles 1 year after implantation seems surprising. Yet, these findings are in concert with previously published long term human data.17, 18 Finally, our specimens indicate that long term implantation of durapatite did not enhance attachment regeneration per se. Regarding citric acid root treatment, no significant cementogenesis was seen supracrestally in our specimens. Our long term data thus support previously published short term results33 in which citric acid root treatment did not enhance supracrestal cementogenesis. Unfortunately, our present specimens do not provide clear evidence indicating whether or not citric acid root treatment potentiates new attachment within the confines of an intraosseous lesion.

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