Periodontal Regeneration and Reconstructive Surgery

Richard T. Kao, Henry H. Takei, David L. Cochran and Marc L. Nevins

When the periodontium is damaged by inflammation or as a result of surgical treatment, the defect heals either through periodontal regeneration or repair.* In periodontal regeneration, healing occurs through the reconstitution of a new periodontium, which involves the formation of alveolar bone, functionally aligned periodontal ligament, and new cementum. Alternatively, repair due to healing by replacement with epithelial and/or connective tissue that matures into various nonfunctional types of scar tissue, is termed new attachment. Histologically, patterns of repair include long junctional epithelium, ankylosis, and/or new attachment (see Chapter 1). Although the stability of periodontal repair is not clear, the ideal goal of periodontal surgical therapy is periodontal regeneration.

This chapter summarizes our current understanding of therapy that results in periodontal regeneration and examines how regenerative approaches used for correcting intrabony defects have changed over the years.

Assessment of Periodontal Wound Healing

It is sometimes difficult in clinical and experimental situations to determine whether regeneration or new attachment has occurred and the extent to which it has occurred. Although there are various evidences of reconstruction, the proof of principle for the type of healing is determined by histological studies. Once defined, the evidence found subsequently by clinical, radiographic, and surgical reentry findings is implied.35,37,166 All these methods have advantages and shortcomings that should be well understood and considered in individual cases and when critically evaluating the literature. A comparative analysis of regenerative approaches is detailed in Table 61-1.

TABLE 61-1

Comparative Analysis of Regenerative Approaches

Graft Material	CAL Gain (mm)	Defect Fill (% or mm)	Histologic Assessment	Comments
Autologous
Extraoral (iliac crest)	3.3-4.2²⁵⁹ • 2.60 mm in 0-wall • 3.75 mm in 1-wall • 4.16 mm in 2-wall

— 33 of 39 defects showed evidence of regeneration⁴⁸ Only evidence of regeneration in 0-wall and (2.5 mm) supracrestal regeneration.
Only one controlled study with 2.98 mm of bone gain vs. 0.66 mm with debridement.⁵¹
No significant difference in one study. ⁵⁴ Intraoral autologous 2.88-3.44 mm^34,^73,^75,¹¹⁷ 73%⁵¹ 0.7 mm of regeneration^48,55 Allograft (vital) Human vital 3.6 mm mean²⁵⁹

• 3.6 mm in 1-, 2-, and 3-wall

• 2.1 mm in 0-wall

— Evidence of regeneration⁴⁸ Potential risk of disease transmission Allograft (nonvital) FDBA 2.0 mm mean^174,^179,^256,²⁷⁶ 60%-68% of 1401 defects had >50% fill^61–64 None available Only controlled study using paired defects show no difference between FDBA vs. debridement.⁶⁵
No histological study of healing pattern.
The addition of autologous osseous coagulum enhances healing. Comparative Studies FDBA vs. FDBA + autologous graft — 63%-67% had >50% fill
78%-80% had >50% fill⁶² Allograft (non-vital) DFDBA vs. debridement 2.3-2.9 mm vs. 0.3-1.3 mm^177,²¹⁷ 65% vs. 11%^72–74 1.21mm of periodontal regeneration^70,⁷¹ Comparative Studies DFDBA vs. FDBA 1.7 vs. 2.4 mm²⁵² 59% vs. 66%⁷⁵ Ceramics HA vs. debridement 1.3-2.8 mm vs. 0.5-0.9 mm^171,329,330 67% vs. 10%⁹¹ No new periodontal attachment, osteogenesis, or centogenesis⁹⁷ PHA vs. debridement 3.6 mm vs. 1.2 mm¹³⁹ 55%-60% vs. 23%
had > 50% fill⁹²^–⁹⁴ Bone formation in the implant pores and periphery. No new attachment. Pocket reduction by long JE.^104–106 TCP 2.3-2.7 mm^33,^140,²⁸⁸ 24 mm vs. 9 mm¹⁰⁰
58 mm vs. 22 mm¹⁰¹
67%¹⁰⁷ Fibrous encapsulation followed by rapid resorption. No evidence of new attachment. Healing by long JE.¹¹² Calcium Carbonates NCS vs. debridement 2.3 mm vs. 0.7 mm 67% vs. 26%¹²¹ NCS is superior to debridement. GTR ePTFE 2.0-5.3 mm^51,92,315 0.5-1.7 mm of new attachment Resorbable barrier
polyglactin-910 vs. ePTFE 4.0 mm vs. 3.5 mm^42,⁴³ 77.5% vs. 70.7%^167,168 Comparative Studies ePTFE + DFDBA + citric acid root conditioning 4.7 mm²⁶³ Clinical series suggest improved results with DFDBA + citric acid root conditioning. ePTFE vs. ePTFE + HA-collagen graft vs. HA-collagen graft vs. debridement 3.70 mm¹⁴¹
3.80 mm
2.60 mm
2.1 mm 1.50 mm¹⁴¹
1.55 mm
0.85 mm
0.60 mm ePTFE membranes ± HA-collagen was better than HA-collagen or debridement. EMDs EMD vs. placebo control or debridement 2.2 mm vs 1.7mm¹¹³
4.28 mm vs 2.65mm⁷⁸ —
74.0% vs. 22.7%¹⁹⁶ Histological analysis of 2 cases. Both cases had new cementum and attachment but only one had new bone.^191,¹⁹² Suggests EMD can stimulate new attachment. Comparative Studies EMD vs. GTR
(evaluate after 24 and 48 months) 3.0 mm vs. 2.9mm²⁶⁶
2.9 vs. 3.1mm²²⁶ — Both techniques improve CAL; comparable results and appear to be stable over 4 years. EMD vs. DFDBA 3.2 vs. 3.0 mm⁹⁸ — Improved results over published debridement results but no difference between treatment modality. EMD + anorganic bone vs. EMD + fibrin glue 2.89 vs. 2.83mm¹⁵⁹ rhPDGF + β-TCP rhPDGF+ β-TCP vs. placebo (pivotal trail 6-month data) 3.8 vs 3.3mm²⁰³ 57% vs. 18%
LBF: 2.6 mm vs. 0.9 mm rhPDGF + β-TCP vs. placebo (pivotal trail 36-month data) 4.3 vs. 3.2mm²⁰⁴ 60.5% vs. 32.6%
LBF 2.88 mm vs. 1.42 mm Maximum regeneration seen with 0.3 mg/mL rhPDGF was at the 1-year mark and the results were stable.

CAL, clinical attachment level; DFDBA, Demineralized freeze-dried bone allograft; EMD, enamel matrix derivative; ePTFE, expanded polytetrafluoroethylene; FDBA, freeze-dried bone allograft; GTR, guided tissue regeneration; HA, hydroxyapatite; JE, junctional epithelium; LBF, linear bone fill; NCS, calcium carbonates; PHA, porous hydroxyapatite; rhPDGF, recombinant human platelet-derived growth factor; TCP, tricalcium phosphate.

Histological Methods

It is only through histological analysis can one define the nature of the reparative tissue (Figure 61-1). In periodontal reconstructive surgery, the goal is to achieve periodontal regeneration. Classically, experimental animal model systems^36,213 are used whereby reference notches are placed at the base of bony defects or at the apical extent of calculus deposits. Periodontal regeneration is considered to have occurred when the newly formed functionally aligned periodontium is coronal to the apical extent of the notches. Reparative tissue response dominated may include long junctional epithelium, connective tissue adhesion, and root resorption associated with ankylosis. It should be noted that the healing may be predominated by periodontal regeneration; there may be localized areas of repair.²³³ Unfortunately, this approach cannot be used in human studies as it would be unethical to extract the treated tooth, especially when it responded positively to therapy. On rare circumstances, human histology is available if the tooth is to be extracted in conjunction with orthodontic or restorative therapy (Figure 61-2).

Figure 61-1 Possible healing patterns for a periodontal wound, which are dependent on the four possible cell types that predominate that wound site. The downgrowth of epithelial cells (E) results in a long junctional epithelium (JE). The proliferation of connective tissue (CT) may result in connective tissue adhesion ± root resorption. With the predominance of bone cells (B), there is root resorption and/or ankylosis. With the ingress of periodontal ligament (PDL) and perivascular cells from the bone, a regenerated periodontium develops. (Courtesy of Rose L, et al, editor: Periodontics: medicine, surgery, and implants, St Louis, Elsevier Mosby, 2004.)

Figure 61-2 Photomicrographs of a clinical case of periodontal regeneration 9 months after the application of recombinant human platelet derived growth factor. Histological landmarks as evidence of regeneration should include: a low magnification view of the regenerated area (A); a detailed view of the notched root surface (B) and the newly regenerated periodontium coronal to this landmark (C); and the coronal aspect of the regenerated periodontium in relationship to the junctional epithelium (D). Abbreviations: PDL (periodontal ligament), NC (new cementum), NB (new bone), OB (old bone), TR (root trunk), BV (blood vessel), JE (junctional epithelium), and CT (connective tissue). (Courtesy of Dr. S. Lynch Rose L, et al, editor: Periodontics: medicine, surgery, and implants, St Louis, Elsevier Mosby, 2004.)

Clinical Methods

Clinical methods to evaluate periodontal reconstruction consist of comparisons between pretreatment and posttreatment pocket probings and determinations of clinical gingival findings. The probe can be used to determine pocket depth, attachment level, and bone level (Figure 61-3). Clinical determinations of attachment level are more useful than probing pocket depths because the latter may change as a result of displacement of the gingival margin (see Chapter 29).

Figure 61-3 Different types of probings in an interdental space. Several studies have determined that the depth of penetration of a probe in a periodontal pocket varies according to the degree of inflammatory involvement of the tissues immediately beneath the bottom of the pocket (Figure 61-4). Therefore, even though the forces used may be standardized with pressure-sensitive probes, there is an inherent margin of error in this method that is difficult to overcome. Fowler et al⁷¹ have calculated this error to be 1.2 mm, but it is even greater when furcations are probed.

Several studies have determined that the depth of penetration of a probe in a periodontal pocket varies according to the degree of inflammatory involvement of the tissues immediately beneath the bottom of the pocket (Figure 61-4). Therefore, even though the forces used may be standardized with pressure-sensitive probes, there is an inherent margin of error in this method that is difficult to overcome. Fowler et al⁷¹ have calculated this error to be 1.2 mm, but it is even greater when furcations are probed.¹⁸⁹

Figure 61-4 *Left,* Arrow pointing downward depicts penetration of a probe in an untreated periodontal pocket. The probe tip goes past the junctional epithelium and the inflamed tissue and is stopped by the first intact, attached collagen fibers. *Right,* After thorough scaling and root planing, the location of the bottom of the pocket has not changed, but the probe penetrates to only about one-third the length of the junctional epithelium (see Chapter 29). The reduction in probing depth may not reflect a change in attachment level.

Bone probing performed with the patient under anesthesia is not subject to this error and has been found to be as accurate as bone height measurements made on surgical reentry.93,240,311

Measurements of the defect should be made before and after treatment from the same point within the defect and with the same angulation of the probe. This reproducibility of probe placement is difficult and may be facilitated in part by using a grooved stent to guide the introduction of the probe (Figure 61-5). Preoperative and postoperative comparability of probing measurements that do not use this standardized method may be open to question.

Figure 61-5 Grooved acrylic stent used in clinical research to standardize the direction of introduction of the probe.

Radiographic Methods

Radiographic evaluation of periodontal regeneration allows assessment of the bone tissue adjacent to the tooth. This technique also requires carefully standardized techniques for reproducible positioning of the film and the tube.216,249 Even with standardized techniques (see Chapter 31), the radiograph does not show the entire topography of the area before or after treatment. Furthermore, thin bone trabeculae may exist before treatment and go undetected radiographically because a certain minimal amount of mineralized tissue must be present to register on the radiograph. Several studies have demonstrated that radiographs, even those taken with standardized methods, are less reliable than clinical probing techniques.^154,299 A comparative study of pretreatment bone levels and posttherapy bone fill with 12-month reentry bone measurements showed that linear radiographic analysis significantly underestimates pretreatment bone loss and posttreatment bone fill.³⁰⁰

Studies with subtraction radiography have enhanced the usefulness of radiographic evaluation.60,61,317 A comparative study of linear measurement, computer-assisted densitometric image analysis (CADIA), and a method combining the two reported that the linear-CADIA method offers the highest level of accuracy.³⁰³

Surgical Reentry

The surgical reentry of a treated defect after a period of healing can provide a good view of the state of the bone crest that can be compared with the view taken during the initial surgical intervention and can also be subject to measurements (Figure 61-6). Models from impressions of the bone taken at the initial surgery and later at reentry can be used to assess the results of therapy.

Figure 61-6 A, Deep three-wall vertical osseous defect with measuring probe inserted. B, Reentry surgery 9 months after treatment shows repaired bone defect. C, Radiographs before and after treatment showing fill of angular osseous defect; gutta percha points extend to base of pocket. (From Glickman I: Clinical periodontology, ed 3, Philadelphia, 1964, Saunders.)

This method is very useful but has two shortcomings: It requires a frequently unnecessary second procedure, and it does not show the type of attachment that exists (i.e., new attachment or long junctional epithelium ³⁵) (Figure 61-7).

Figure 61-7 A, Periodontal pocket preoperatively. B, Periodontal pocket immediately after scaling, root planing, and curettage. C, New attachment. The arrow indicates the most apical part of the junctional epithelium. Note regeneration of bone and periodontal ligament. D, Healing by long junctional epithelium. Again, the arrow indicates the most apical part of the junctional epithelium. Note that the bone is new, but the periodontal ligament is not.

Reconstructive Surgical Techniques

Reconstructive techniques can be subdivided into three major therapeutic approaches: non–bone graft–associated, graft-associated, and biological mediator–associated new attachment and regeneration. In clinical practice, it is common for clinicians to combine these various approaches.84,104

All recommended techniques include careful case selection and complete removal of all irritants on the root surface. Although this can be done in some cases as a closed procedure, in the great majority of cases, it should be done after exposure of the area with a flap.6,7 Flap design and incisions should follow the description given in Chapter 59 for flaps used in reconstructive surgery. Trauma from occlusion, as well as other factors, may impair posttreatment healing of the supporting periodontal tissues, reducing the likelihood of new attachment. Occlusal adjustment, if needed, is therefore indicated.

Systemic antibiotics are generally used after reconstructive periodontal therapy, although definitive information on the advisability of this measure is still lacking. Case reports have shown extensive reconstruction of periodontal lesions after scaling, root planing, and curettage, with systemic and local treatment using penicillin or tetracycline, in combination with other forms of therapy.32,192

Non–Graft-Associated Reconstructive Procedures

The following sections discuss the rationale and techniques that must be considered for a successful outcome in achieving new attachment or periodontal bone regeneration in response to non–graft-associated reconstructive surgical therapy. Of these procedures, guided tissue regeneration (GTR) is the main procedure used in clinical practice. Recent evidences suggest that laser-assisted new attachment procedure (LANAP) may also result in new attachment and regeneration but further clinical trial are needed to test its efficacy and parameter for success. Additionally, there are several procedures such as (1) the removal of the junctional and pocket epithelium; (2) the prevention of their migration into the healing area after therapy; (3) clot stabilization, wound protection, and space creation; and (4) the biomodification of the root surfaces that are of historical interest. Although these procedures are not used individually as reconstructive approach, much of these strategies are currently incorporated as adjunct for reconstructive surgery.

Guided Tissue Regeneration.

GTR is used for the prevention of epithelial migration along the cemental wall of the pocket and maintaining space for clot stabilization. Derived from the classic studies of Nyman, Lindhe, Karring, and Gottlow, this method is based on the assumption that periodontal ligament and perivascular cells have the potential for regeneration of the attachment apparatus of the tooth.* GTR consists of placing barriers of different types (membranes) to cover the bone and periodontal ligament, thus temporarily separating them from the gingival epithelium and connective tissue. Excluding the epithelium and the gingival connective tissue from the root surface during the postsurgical healing phase not only prevents epithelial migration into the wound but also favors repopulation of the area by cells from the periodontal ligament and the bone³⁸ (see also Chapter 1). It should be noted that in the United States, GTR is often performed with some type of bone graft as a scaffolding agent, so it is a combined therapy. In Europe and other parts of the world where regulatory and religious constraints makes human graft materials unavailable, so it is performed as a traditional GTR procedure and may be occasionally used in conjunction with a other graft materials as a combined therapy.

Initial animal experiments using Millipore filters and Teflon membranes resulted in regeneration of cementum and alveolar bone and a functional periodontal ligament.32,34,38,129 Clinical case reports indicate that GTR results in a gain in attachment level.^17,18 Histologic studies in humans provided evidence of periodontal reconstruction in most cases, even with horizontal bone loss.^90,290,292

The use of polytetrafluoroethylene (PTFE) membranes has been tested in controlled clinical studies in mandibular molar furcations and has shown statistically significant decreases in pocket depths and improvement in attachment levels after 6 months, but bone level measurements have been inconclusive.158,225 A study on maxillary molar furcations did not result in significant gain in attachment or bone levels.¹⁸²

With the regenerative success associated with the use of nonresorbable membrane, the advantage and disadvantage of this approach became apparent. Notably, problems such as membrane exposure, which resulted in no or limited regeneration and the need for a secondary procedure for surgical removal resulted in the development of biodegradable membranes.²⁷⁴ Today in clinical practice, most GTR procedures use biodegradable membranes while the nonresorbable membranes are used for implant site development. Nevertheless, the historical research using nonresorbable membranes and the development of various types of biodegradable membranes is valuable.

Nonresorbable Membranes.

In classic animal and human studies demonstrating the efficacy of GTR, cellulose acetate filters were used. As this technique became more prevalent, the first commercial membrane was produced from expanded polytetrafluoroethylene (ePTFE). This membrane has all the properties necessary for GTR barriers in that it (1) is a cellular barrier; (2) is biocompatible; (3) provides space for the healing tissue; (4) permits tissue integration; and (5) is clinically manageable. Much of our current understanding of GTR is based on studies using ePTFE membranes. Although they are used less frequently now, they are still popular for guided bone regeneration and ridge preservation, so it is important to understand the clinical procedures for managing these membranes.

The clinical effectiveness of ePTFE membranes is dependent on technique. Preservation of the keratinized gingiva and a relatively thick overlying surgical flap are critical to avoid perforation of the flap by the membrane during healing. After the surgical area has been flapped, the defect is degranulated and the root surface scaled and root planed. The ePTFE membrane is trimmed to adapt to tooth configuration, secured by ePTFE sutures, and the flap repositioned. It is interesting to note that, although much of the emphasis in the literature is on adapting the membrane to the defect, no membrane can ever be perfectly adapted. Despite gaps, these membranes seem to work. After membrane placement, healing is allowed to proceed for 4 to 6 weeks. Barring any membrane exposure, a second surgery is performed to remove the membrane. During this removal, the healing tissue appears reddish and granulomatous. After membrane removal, the area should not be probed for 3 months. Radiographic evidence of bone fill is usually present after 6 months and should continue over the course of 1 year (Figure 61-8).

Figure 61-8 Radiographs of a guided tissue regeneration (GTR) case using a non-resorbable expanded polytetrafluoroethylene (ePTFE) membrane. The mesially inclined molar is associated with a three-walled intraosseous defect **(A, B)**. The defect was filled with demineralized freeze-dried bone allograft (DFDBA) and ePTFE was used. Membrane was exposed after 8 weeks and removed 2 weeks later. Radiographic “fill” was halfway after 6 months and maximum fill was present after 12 months **(C)** with minimal probing depth. (Courtesy of Rose L, et al, editor: Periodontics: medicine, surgery, and implants, St Louis, Elsevier Mosby, 2004.)

Clinical studies have shown that ePTFE membranes used in GTR procedures are more effective than surgical debridement in correcting intrabony defects.* In intrabony and furcation defects, there are gains in clinical attachment level (3 to 6 mm), improved bone levels (2.4 to 4.8 mm), and probing depth reductions (3.5 to 6 mm). Studies have demonstrated that these regenerative results can be maintained over the course of several years.^{51,92,263,315}

The advent of titanium-reinforced ePTFE allowed for the formation of larger spaces, thus permitting correction of larger defects (Figure 61-9).⁵⁰ This resulted in significant clinical improvements using titanium-reinforced ePTFE compared to ePTFE.

Figure 61-9 Clinical photographs and radiographs of a guided tissue regeneration case using expanded polytetrafluoroethylene (ePTFE) with titanium-reinforced membrane. The osseous defect was along the distal interproximal area wrapping buccally over the furcation **(A, B)**. To prevent the membrane from collapsing over the root surfaces, demineralized freeze-dried bone allograft (DFDBA) and adjusting the titanium membrane provide a larger space for regeneration **(C, D)**. One year afterward, the radiographic and clinical signs are consistent with achieving regeneration in this defect (E). (Courtesy of Rose L, et al, editor: Periodontics: medicine, surgery, and implants, Elsevier Mosby, 2004.)

To determine how regeneration can be enhanced with GTR technique, the prolonged retention of ePTFE membranes was evaluated.¹⁹⁶ After allowing the membrane to be retained for 4 months, surgical re-entry after 1 year determined that the mean bone fill of intrabony defects was 95%. This suggests that prolonged retention of a barrier membrane is desirable if no tissue perforation is present. This is consistent with many clinical reports of the improved bone quality associated with guided bone regeneration in implant site development.

The major problem with using non-resorbable membranes is that the membrane is exposed to the oral environment during healing. Upon exposure, the membrane is contaminated and colonized by oral microflora.187,206,213,281 Several studies have shown that contamination of the surgical field can result in decreased formation of new attachment. If the membrane is exposed, the infection can be temporarily managed with topical application of chlorhexidine. This may minimize the infection and extend the time the membrane can be retained in place.

Biodegradable Membranes.

Bioresorbable membranes have replaced the routine use of ePTFE membranes in guided tissue regeneration. There are basically three types of bioresorbable membranes: (1) polyglycoside synthetic polymers (i.e., polylactic acid, polylactate/polygalactate co-polymers), (2) collagen, and (3) calcium sulfate. Polyglycoside membranes degrade as the result of random nonenzymatic cleavage of the polymer, producing polylactide and polyglycolide, which are converted to lactic acid and pyruvate, respectively, and metabolized by the enzymes of the Krebs cycle. Porcine collagen membranes are degraded by collagenases and subsequently by gelatinases and peptidase. There has been a resurgence in the use of calcium sulfate as a regeneration material because it can be used as a pavable resorbable barrier when used in combination with bone or bone substitutes. The calcium sulfate is bioresorbed through a giant cell reaction. Several features make these bioresorbable membranes easier to manage clinically: (1) they are more tissue compatible than nonresorbable membranes; (2) the timing for resorption can be regulated by the amount of cross-linkage in the synthetic polymer and collagen membrane or the amount of heat-processed calcium sulfate chips in calcium sulfate barrier; and (3) a second surgical procedure is not required to retrieve the nonresorbable membrane.

A recent GTR study compared the use of bioresorbable membranes (polylactate/polygalactate copolymer) versus ePTFE membranes, with surgical debridement as a control.⁵² After 1 year, significant gains in clinical attachment level (CAL) were observed in all three groups. There was no difference in CAL gain between the two membrane groups, with both of them gaining 2 mm or more. In both membrane groups, 83% of the sites improved 4 mm or more, which was significantly better than the surgical debridement control group. These findings indicate GTR procedures are equally effective using resorbable and nonresorbable membranes. This finding has been confirmed by other investigators.^42,43,316

A large multicenter clinical study reported the use of bioresorbable membranes in 203 consecutively treated intrabony defects.⁶⁶ After 1 year, investigators found that CAL improved by 79%, and 78% of the sites improved by 4 mm or more. An average of 3 mm of bone fill was measured radiographically. Compromised clinical results occurred in incidences in which membranes were exposed or patients had poor plaque control.

The search for resorbable membranes has included trials and tests with numerous materials and collagens from different species such as bovine, porcine, Cargile membrane derived from the cecum of an ox, polylactic acid, Vicryl (polyglactin 910), synthetic skin (Biobrane), and freeze-dried dura mater.* Clinical studies with a mixture of copolymers derived from polylactic acid and acetyl tributyl citrate resorbable membranes (Guidor membrane, no longer on the market) and a poly-d,l-lactide-co-glycolide (Resolut membrane, also no longer on the market) have shown significant gains in clinical attachment and bone fill.^43,68,198

The potential of using autogenous periosteum as a membrane and also to stimulate periodontal regeneration has been explored in two controlled clinical studies, one of grade II furcation involvements in mandibular molars and another of interdental defects.153,157 The periosteum was obtained from the patient’s palate by means of a window flap. Both studies reported that autogenous periosteal grafts can be used in GTR and result in significant gains in clinical attachment and osseous defect fill.

Laser-Assisted New Attachment Procedure.

The role of laser in periodontal therapy remains controversial (see Chapter 65). Nevertheless, the use of neodymium : yttrium-aluminum-garnet (Nd : YAG) to perform surgical LANAPs has been reported for the management of chronic periodontitis^138,186 and can potentially result in new attachment and periodontal regeneration (see Chapter 65).^201,334

Many questions remain about LANAP that need to be clarified. The first is the exact mechanism and parameter by which healing by new attachment versus regeneration occur with LANAP therapy. Additionally, a blinded split mouth study to compare LANAP protocol to other existing periodontal therapies is in progress and needs to be completed. This along with other randomized controlled trials will be needed for meta-analysis to determine if LANAP is equivalent or superior to other conventional therapy. As with all periodontal therapy, the long-term stability of the regeneration need to be explored.

Non–Graft-Associated Procedures of Historical Interest

Removal of Junctional and Pocket Epithelium.

Since the earliest attempts at periodontal new attachment, the presence of junctional and pocket epithelium has been perceived as a barrier to successful therapy because its presence interferes with the direct apposition of connective tissue and cementum, thus limiting the height to which periodontal fibers can insert to the cementum.86,131,156,212 Several methods have been recommended to remove the junctional and pocket epithelium. These include curettage, chemical agents, ultrasonics, lasers, and surgical techniques.

Curettage.

Results of removal of the epithelium by means of curettage vary from complete removal to persistence of as much as 50%.²⁸³ Though curettage is not a reliable procedure, occasional bone regeneration does occur (Figure 61-10). Ultrasonic methods, lasers, and rotary abrasive stones have also been used, but their effects cannot be controlled because of the clinician’s lack of vision and tactile sense when using these methods.

Fibronectin.

Fibronectin is the glycoprotein that fibroblasts require to attach to root surfaces. The addition of fibronectin to the root surface may promote new attachment.28,69,297 However, increasing fibronectin above plasma levels produces no obvious advantages. Adding fibronectin and citric acid to lesions treated with GTR in dogs did not improve the results.^29,284

Tetracycline.

In vitro treatment of the dentin surfaces with tetracycline increases binding of fibronectin, which in turn stimulates fibroblast attachment and growth while suppressing epithelial cell attachment and migration.287,298 Tetracycline also removes an amorphous surface layer and exposes the dentin tubules. In vivo studies, however, have not shown favorable results.^318,319 A human study showed a trend for greater connective tissue attachment after tetracycline treatment of roots. Tetracycline gave better results when used alone than when combined with fibronectin.³ Tetracycline has been used as an adjunctive procedure in preparation of the root in regenerative procedures and is recommended step for use with biologic mediators.

Surgical Techniques.

Surgical techniques have been recommended to eliminate the pocket and junctional epithelium. The excisional new attachment procedure (ENAP) consists of an internal bevel incision performed with a surgical knife, followed by removal of the excised tissue.³²⁸ No attempt is made to elevate a flap. After careful scaling and root planing, interproximal sutures are used to close the wound (see Chapter 56). This approach has been modified and is used in conjunction with the Nd : YAG laser in the previously described LANAP procedure.

Glickman ⁸⁸ and Prichard²²⁸ have advocated performing a gingivectomy to the crest of the alveolar bone and debriding the defect. Excellent results have been obtained with this technique in uncontrolled human studies.^16,230

The modified Widman flap, as described by Ramfjord and Nissle,²³⁴ is similar to the excisional new attachment procedure but is followed by elevation of a flap for better exposure of the area. The internal bevel incision eliminates the pocket epithelium (see Chapter 59).

Preventing or Impeding the Epithelial Migration.

Elimination of the junctional and pocket epithelium may not be sufficient because the epithelium from the excised margin may rapidly proliferate to become interposed between the healing connective tissue and the cementum.

For experimental purposes, several investigators have analyzed in animals and humans the effect of excluding the epithelium by amputating the crown of the tooth and covering the root with the flap (“root submergence”).19,20,22,39 This experimental technique not only excludes the epithelium but also prevents microbial contamination of the wound during the reparative stages. Successful repair of osseous lesions in the submerged environment was reported, but obviously this method has little or no clinical application.

Two other methods have been proposed to prevent or impede the migration of the epithelium. One consists of the total removal of the interdental papilla covering the defect and its replacement with a free autogenous graft obtained from the palate.⁶³ During healing, the graft epithelium necroses and is slowly replaced by proliferating epithelium from the gingival surface. The graft simply delays the epithelium from proliferating into the healing area. This method has not been widely used.

The second approach is the use of coronally displaced flaps, which increase the distance between the epithelial wound edge and the healing area. This technique is particularly suitable for the treatment of mandibular molar furcations and has been used mostly in conjunction with citric acid treatment of the roots.81,167 Periodontal regeneration after the use of this technique has been demonstrated histologically in humans.²⁷⁶

Clot Stabilization, Wound Protection, and Space Creation.

Some investigators have attributed the successful results reported with graft materials, barrier membranes, and coronally displaced flaps to the fact that these techniques protect the wound and create a space for undisturbed and stable maturation of the clot 83,156,157 This hypothesis suggests that preservation of the root surface fibrin clot interface prevents apical migration of the gingival epithelium and allows for connective tissue attachment during the early wound-healing period.^83,213,223

The importance of space creation for bone repair has long been recognized in orthopedic and maxillofacial surgery. Transference of this concept to periodontal therapy has been explored for treatment of periodontal and periimplant osseous defects and for root coverage. The space can be created by using a titanium-reinforced ePTFE membrane to prevent its collapse. For the study of reconstructive techniques, these membranes were placed over experimentally created supraalveolar bone defects in dogs, and considerable bone reconstruction was reported.²⁷⁸ The following is a discussion of the guided tissue regeneration technique.

Graft Materials and Procedures

Numerous therapeutic grafting modalities for restoring periodontal osseous defects have been investigated. Periodontal reconstruction can be attained without the use of bone grafts in meticulously treated three-wall defects (intrabony defects) and in periodontal and endodontic abscesses.32,116,137,230 New attachment is more likely to occur when the destructive process has occurred rapidly, such as after treatment of pockets complicated by acute periodontal abscesses and after treatment of acute necrotizing ulcerative lesions.¹⁹⁷ The use of graft materials at one time was to provide regenerative inductive effect but should be viewed primarily as providing a scaffold for healing.

The following classifications of bone graft material are important to note. Grafts are either categorized by their origins and function during healing. Categorization by origin include: (1) autografts are bone obtained from the same individual; (2) allografts are bone obtained from a different individual of the same species; and (3) xenografts are bone from a different species. Bone graft materials are also evaluated based on their osteogenic, osteoinductive, or osteoconductive potential. Osteogenesis refers to the formation or development of new bone by cells contained in the graft. Osteoinduction is a chemical process by which molecules contained in the graft (e.g., bone morphogenetic proteins) convert the neighboring cells into osteoblasts, which in turn form bone. Osteoconduction is a physical effect by which the matrix of the graft forms a scaffold that favors outside cells to penetrate the graft and form new bone.

Periodontal defects as sites for transplantation differ from osseous cavities surrounded by bony walls. Saliva and bacteria may easily penetrate along the root surface, and epithelial cells may proliferate into the defect, resulting in contamination and possible exfoliation of the grafts. Therefore the principles established to govern transplantation of bone or other materials into closed osseous cavities are not fully applicable to transplantation of bone into periodontal defects.⁶²

Schallhorn ²⁶² defined the considerations that govern the selection of a material as follows: biologic acceptability, predictability, clinical feasibility, minimal operative hazards, minimal postoperative sequelae, and patient acceptance. It is difficult to find a material with all these characteristics, and to date, there is no ideal material or technique.

Graft materials have been developed and tried in many forms. To familiarize the reader with various types of graft material, as defined by either the technique or the material used, a brief discussion of each is provided.

All grafting techniques require presurgical scaling, occlusal adjustment as needed, and exposure of the defect with a full-thickness flap. The flap technique best suited for grafting purposes is the papilla preservation flap because it provides complete coverage of the interdental area after suturing (see Chapter 57). The use of antibiotics after the procedure is generally recommended.

Autogenous Bone Grafts

Bone from Intraoral Sites.

In 1923, Hegedüs ¹¹² attempted to use bone grafts for the reconstruction of bone defects produced by periodontal disease. The method was revived by Nabers and O’Leary¹⁹⁸ in 1965, and numerous efforts have been made since that time to define its indications and technique.

Sources of bone include bone from healing extraction wounds, bone from edentulous ridges, bone trephined from within the jaw without damaging the roots, newly formed bone in wounds especially created for the purpose, bone removed from tuberosity, and the ramus and bone removed during osteoplasty and ostectomy.34,103,116,117,246,327

Osseous Coagulum.

Robinson described a technique using a mixture of bone dust and blood that he termed “osseous coagulum.”²⁴⁶ The technique uses small particles ground from cortical bone. The advantage of the particle size is that it provides additional surface area for the interaction of cellular and vascular elements.

Sources of the graft material include the lingual ridge on the mandible, exostoses, edentulous ridges, the bone distal to a terminal tooth, bone removed by osteoplasty or ostectomy, and the lingual surface of the mandible or maxilla at least 5 mm from the roots. Bone is removed with a carbide bur #6 or #8 at speeds between 5000 and 30,000 rpm, placed in a sterile dappen dish and used to fill the defect (Figure 61-11). The obvious advantage of this technique is the ease of obtaining bone from an area already exposed during surgery. The disadvantages are its relatively low predictability and the inability to procure adequate material for large defects.⁶³ Although notable success has been reported by many individuals, studies documenting the efficacy of the technique are still inconclusive.^53,74,79,245

Figure 61-11 A, Osseous defect mesial to a second premolar. B, Graft material placed in dappen dish before transfer to the graft site. C, Material in place. D, Reentry 6 months later. (Courtesy Dr. E. Earl Robinson.)

Bone Blend.

Some disadvantages of osseous coagulum derive from the inability to use aspiration during accumulation of the coagulum. Another problem is the unknown quantity and quality of the bone fragments in the collected material. To overcome these problems, the “bone blend technique” has been proposed.⁵⁶

The bone blend technique uses an autoclaved plastic capsule and pestle. Bone is removed from a predetermined site, triturated in the capsule to a workable, plasticlike mass, and packed into bony defects. Froum et al 73–75 found osseous coagulum–bone blend procedures to be at least as effective as iliac autografts and open curettage.

Cancellous Bone Marrow Transplants.

Cancellous bone can be obtained from the maxillary tuberosity, edentulous areas, and healing sockets.¹¹⁰ The maxillary tuberosity frequently contains abundant cancellous bone, particularly if the third molars are not present. After a ridge incision is made distally from the last molar, bone is removed with a curved rongeur. Care should be taken not to extend the incision too far distally to avoid entering the mucosal tissue of the pharyngeal area. Also, the location of the maxillary sinus must be analyzed on the radiograph to avoid entering or disturbing it.

Edentulous ridges can be approached with a flap, and cancellous bone and marrow are removed with curettes, back-action chisels, or trephine. Extraction sockets are allowed to heal for 8 to 12 weeks before reentering and removing the newly formed bone from the apical portion, which is used as the donor material.

Bone Swaging.

The bone swaging technique requires an edentulous area adjacent to the defect, from which the bone is pushed into contact with the root surface without fracturing the bone at its base.65,251 Bone swaging is technically difficult, and its usefulness is limited.

Bone from Extraoral Sites.

In 1923, Hegedüs also pioneered the use of extraoral sites as a source of bone for grafting into periodontal osseous defects, using bone from the tibia. Schallhorn and Hiatt revived this approach in the 1960s using the iliac crest (see next discussion).

The use of fresh or preserved iliac cancellous marrow bone has been extensively investigated. This material has been used by orthopedic surgeons for years. Data from human and animal studies support its use, and the technique has proved successful in osseous defects with various numbers of walls. It has also been successful in furcations and even supracrestally to some extent.10,26,58,259,260 However, because of numerous problems associated with its use, the technique is no longer in use.²⁶⁰ Some of the problems were postoperative infection, bone exfoliation, sequestration, varying rates of healing, root resorption, and rapid recurrence of the defect (Figure 61-12). Other problems were increased patient expense and difficulty in procuring the donor material.^{22,50,174,175}

Figure 61-12 A, November 1973: Radiograph of a patient immediately before placement of a fresh iliac autograft. B, Two months later, bone repair is evident. Note the early radiolucent areas on the mesial aspect of the canine. C, After 7 months, “bone fill” is occurring, but obvious root resorption is present. D, April 1975: Root resorption is apparent on all grafted teeth. Note the obvious degree of fill of the original bone defects. E, February 1976: Further involvement. F, October 1977: Four years later, root resorption has progressed into the pulp of the lateral incisor, causing a periosteal-endosteal complication.

Bone Allografts.

Obtaining donor material for autograft purposes necessitates inflicting surgical trauma on another part of the patient’s body. Obviously, it would be to the patient’s and therapist’s advantage if a suitable substitute could be used for grafting purposes that would offer similar potential for repair and not require the additional surgical removal of donor material from the patient. However, both allografts and xenografts are foreign to the patient and, therefore, have the potential to provoke an immune response. Attempts have been made to suppress the antigenic potential of allografts and xenografts by radiation, freezing, and chemical treatment.²⁵

Bone allografts are commercially available from tissue banks. They are obtained from cortical bone within 12 hours of the death of the donor, defatted, cut in pieces, washed in absolute alcohol, and deep-frozen. The material may then be demineralized, and subsequently ground and sieved to a particle size of 250 to 750 µm and freeze-dried. Finally, it is vacuum-sealed in glass vials.

Numerous steps are also taken to eliminate viral infectivity. These include exclusion of donors from known high-risk groups and various tests on the cadaver tissues to exclude individuals with any type of infection or malignant disease. The material is then treated with chemical agents or strong acids to inactivate the virus, if still present. The risk of human immunodeficiency virus (HIV) infection has been calculated as 1 in 1 to 8 million and is therefore characterized as highly remote.¹⁷⁸

Freeze-Dried Bone Allograft.

Several clinical studies by Mellonig, Bowers, and coworkers reported bone fill exceeding 50% in 67% of the defects grafted with freeze-dried bone allograft (FDBA) and in 78% of the defects grafted with FDBA plus autogenous bone.174,198,256,276 FDBA, however, is considered an osteoconductive material, whereas demineralized FDBA (DFDBA) is considered an osteoinductive graft. Laboratory studies have found that DFDBA has a higher osteogenic potential than FDBA and is therefore preferred.^175,176,179

Demineralized Freeze-Dried Bone Allograft.

Experiments by Urist 307–310 have established the osteogenic potential of DFDBA. Demineralization in cold, diluted hydrochloric acid exposes the components of bone matrix, which are closely associated with collagen fibrils and have been termed bone morphogenetic proteins (BMPs).^41,309

In 1975, Libin et al ¹⁶¹ reported three patients with 4 to 10 mm of bone regeneration in periodontal osseous defects. Subsequent clinical studies were made with cancellous DFDBA and cortical DFDBA.^217,231 The latter resulted in more desirable results (2.4 mm versus 1.38 mm of bone fill).

Bowers et al,²² in a histologic study in humans, showed new attachment and periodontal regeneration in defects grafted with DFDBA. Mellonig et al^175,176,177 tested DFDBA against autogenous materials in the calvaria of guinea pigs and showed it to have similar osteogenic potential.

These studies provided strong evidence that DFDBA in periodontal defects results in significant probing depth reduction, attachment level gain, and osseous regeneration. The combination of DFDBA and GTR has also proved to be very successful 9,263; however, limitations of the use of DFDBA include the possible, although remote, potential of disease transfer from the cadaver.

A bone-inductive protein isolated from the extracellular matrix of human bones, termed osteogenin or BMP-3, has been tested in human periodontal defects and seems to enhance osseous regeneration.²³ This bone inductive protein is discussed later in this chapter.

Xenografts.

Bone products from other species have a long history of use in periodontal therapy. A few of these xenograft products are mentioned here for historic purposes but are no longer used today. It should be noted that bovine-derived bone (Bio-Oss) is used in combination with GTR for periodontal regeneration mainly in Europe. This material is also used in combination with autologous bone for ridge augmentation.

Calf bone (Boplant), treated by detergent extraction, sterilized, and freeze-dried, has been used for the treatment of osseous defects.10,258 Kiel bone is calf or ox bone denatured with 20% hydrogen peroxide, dried with acetone, and sterilized with ethylene oxide. Anorganic bone is ox bone from which the organic material has been extracted by means of ethylenediamine; it is then sterilized by autoclaving.¹⁷³ These materials have been tried and discarded for various reasons.

Currently, an anorganic, bovine-derived bone marketed under the brand name Bio-Oss (Osteohealth) has been successfully used both for periodontal defects and in implant surgery. It is an osteoconductive, porous bone mineral matrix from bovine cancellous or cortical/>

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