Four cases of peri-implant bone loss associated with undiagnosed necrotic pulps of adjacent teeth are reported. In two cases, bone was obliterated along sinus tracts (fistulas) that coursed between the implant and adjacent tooth. Endodontic treatment was completed on the adjacent teeth concurrent with periapical surgery to seal the tooth apex. The sinus tract (fistula) was excised, and the implant plus tooth surfaces were treated with a combination of concentrated citric acid and 4.3% sodium fluoride solutions. The third case involved peri-implant surgery with endodontic treatment on the adjacent tooth. A fourth case represented an infected socket augmentation which was surgically treated, augmented with microcrystalline fluorapatite in the range of a 300 µm to 400 µm cluster, and allowed to heal for 4 months followed by a trephine bone biopsy and subsequent analysis for bone growth around the fluoridated nonceramic microcrystalline hydroxyapatite (HA). An augmentation procedure employing fluoridated of resorbable HA was then completed. Histologic analysis showed healthy bone regeneration suggesting that therapeutic fluoride treatment and resultant fluorapatite were helpful in inhibiting reinfection following surgical treatment. All 4 infected implant sites were successfully managed and retained using the aforementioned treatment schemes, and there was no evidence of posttreatment infection in any of the 4 cases. It is proposed that fluoride treatment, through the use of 4.3% sodium fluoride and/or fluoridated hydroxyapatite (fluorapatite), shows promise as an adjunctive treatment component in inhibiting peri-implant infection and reinfection when managing ailing or failing implants.
Many cases of peri-implant bone loss have been reported that can be attributed to a variety of traditional causes such as endodontic failure, a periapical lesion of an adjacent tooth, impingement by the implant into an adjacent root of an adjacent tooth, periodontal pathogens seeding into the area, over-heating the bone, implant contamination, and epithelial cells being forced into the peri-implant area.1–9 Bone loss could result in secondary damage to adjacent teeth during the implant procedure through the over-heating of bone during surgery, but in case reports of such, radiographs show the presence of considerable and adequate bone mass between the implant and adjacent teeth rendering this possibility as unlikely. Another possible culprit for postimplant bone loss is that the blood supply to adjacent teeth might be compromised if placement of implants interfered with afferent arterioles that supply affected teeth. Without any methods for identifying the exact supply course of these arterioles that supply the teeth, it is difficult to determine what affect, if any, such impingement might cause. Since most afferent vessels that supply teeth anastomose freely with the collateral blood supply, it is doubtful that damage to one arteriolar blood supply source would be sufficient to compromise the overall regional blood supply to the extent that this would cause necrosis of an adjacent tooth. Also, it must be noted that in reported cases of suspect adjacent teeth, subsequent endodontic procedures have shown that the pulps were totally necrotic, indicating they had probably been nonvital for a prolonged period of time. Fortunately, even though cases of surgical injury to teeth during implant procedures are possible, they are difficult to anticipate, rare, and as such, represent only a few cases per year.
Many investigations reported within the world literature support the fact that fluoride ion is efficacious in preventing dental caries and inhibits many types of oral bacteria, including the Treponemas,10 which have been implicated along with the several species of bacteria in the pathogenesis of periodontal disease. With regard to bone augmentation, it is clear that the surgical microenvironment should be as free of bacterial contamination as possible in order to achieve ideal conditions for conversion of augmentation material to healthy, new bone formation. If oral bacteria are allowed to gain a foothold, microenvironmental infection and lowered pH will exert a powerful inhibitory effect on new bone formation, rendering bone morphogenesis difficult, if not impossible. If the fluoride ion could be introduced specifically into the sensitive microenvironment that is so vulnerable to infection, it is theorized that its presence would inhibit the acid-forming bacteria and prevent local infection,11 thus allowing osteogenesis to proceed to completion with normal healing.
Fluorapatite (FA) is a very insoluble mineral in a neutral solution. However, in the presence of acid, fluoride and phosphate become liberated and are thus dissolved into solution. Normal tissue is neutral to slightly basic. Since dissolution of fluoride from FA requires a lowering of the pH, FA would seem an ideal delivery molecule for inhibitory fluoride ions during incipient stages of infection when bacteria colonize and begin to acidify their local microenvironment and produce biofilms.12–14 When used in conjunction with treatment of a bone-loss scenario, FA would serve as a fluoride source, which would inhibit postsurgical peri-implant infection, thus enhancing conversion of grafted bone in the defect to new viable bone.
ethods and M aterials
A 64-year-old male patient presented to one of the authors' (W.N.) offices for routine implant placement of tooth No. 10 (Figure 1). Within months after implant placement, purulent drainage occurred between the implant and tooth No. 9 (Figure 2). It was determined that tooth No. 9 was nonvital, and a surgical endodontic procedure was completed. The sinus tract that drained between the tooth and implant was curetted, and all associated granulation tissue was removed. The area and implant was cleansed and treated with a combination of concentrated citric acid and 4.3% sodium fluoride solutions. An augmentation procedure was completed employing fluoridated resorbable hydroxyapatite (HA cluster) that resulted in conversion to FA-coated HA (Figure 3). The tissue was sutured (Figure 4) and the implant was bonded to the adjacent teeth for 6 months (Figure 5). The implant survived and bone filled into the void created by surgical treatment of the prior infection (Figure 6).
A 63-year-old male patient presented to one of the authors' (W.N.) offices with mobile tooth No. 25. The tooth was extracted and a 2-stage small-diameter implant was immediately placed into the socket. The tooth was uncovered and finished 5 months later. A sinus tract was noted at the first 6-month follow-up appointment draining from the interproximal area between the implant and the adjacent tooth, No. 26. Periapical radiograph revealed bone loss around the implant and tooth No. 26 (Figure 7). An endodontic procedure was completed on tooth No. 26, and the area between the implant and the tooth was curetted, decontaminated, augmented, and sutured similar to that reported for Case 1 (Figure 8). The bone graft was successful, and the implant was stable 1 year later (Figure 9).
A 65-year-old woman presented to one of the authors' (W.N.) offices for replacement of teeth Nos. 7 through 11 (Figure 10). Implant placement surgery was recommended and was performed without complication. Approximately 4 months subsequent to placement, the patient complained of pain above the No. 7 and 8 implant area. A radiograph revealed bone loss around the peri-implant area of No. 7, 8, and 9 implants (Figure 11). Initially, tooth No. 6 exhibited slight periapical radiolucency (Figure 10) but was judged to be of insufficient concern prior to the implant placement procedure. With subsequent infection at the peri-implant areas, tooth No. 6 became the prime suspect for the source of the problematic infection. Tooth No. 6 was opened and found to be necrotic. An endodontic and peri-apical surgical procedure was completed on tooth No. 6, and the tips of implant Nos. 7, 8, and 9 were sectioned. Granulation tissue was removed and the area was decontaminated and grafted similar to treatment performed for Case 1. The area healed without complication, and a 1-year follow-up radiograph revealed that bone had filled the osseous void (Figure 12).
A 55-year-old man presented to one of the authors' (W.N.) offices with an abscessed tooth that was extracted. The bony defect resulting from tooth extraction plus removal of associated infective granulation tissue (Figure 13), was immediately augmented with FA (Figure 14). The grafting material was allowed to mature for 6 months prior to implant placement (Figure 15). During the osteotomy procedure, a trephine core biopsy was removed from the augmented site. Samples were placed in formalin solution and sent to Dr Jack Lemons (University of Alabama at Birmingham, Center for Metabolic Bone, Birmingham, Ala) for processing and histologic analysis. The specimens were fixed in buffered formalin, transferred, sectioned by Exakt (R&M Biometrics, Nashville, Tenn) processing, and imaged by Bioquant optical microscopy (R&M Biometrics). Histologic evaluation of the samples showed that immature bone formed on the surface and engulfed fluoridated HA crystals identical to that described in the comparable dog studies reported in Nordquist et al14 (Figure 16). Clinical follow-up revealed normal healing and a successful, stable implant.
Cases reported here strongly suggest that subtle, low-grade, chronic infection of adjacent asymptomatic teeth can and do affect the integration process of a dental implant, especially when such teeth are crowned or periodontally involved. Further, this complication is probably much more common than what most implant dentists would suspect. Questioning their own confidence, particularly regarding placement techniques, implant dentists tend to blame the implant design or placement procedures for their clinical failures. They then remove the implant, graft the bone void, and repeat the implant procedure hoping for a better result. Many implant dentists, however, are now becoming more suspicious of these implant failures and are beginning to carefully investigate the viability of adjacent teeth as potential sources of failure. It has been well documented that the surfaces of dental implants are vulnerable to bacterial contamination during the early integration process. Experience has taught clinicians that the implant itself serves as a “dip-stick,” indicating and exposing undiagnosed subclinical infection in the vicinity of a failing implant.
Analyzing these 4 cases, we find that it is difficult to conclude that the bone was burned during the placement of the implants because the treating implant surgeon is highly experienced in both diagnosis and implementation of implant procedures. In addition, there was no evidence of damaging heat produced during any of the surgical steps. It is possible that blood supply was compromised if the implant procedure damaged afferent arterioles supplying affected teeth. However, without any methods for identifying the exact course these arterioles take in supplying the teeth, it is difficult to determine what effect, if any, possible mechanical impingement would cause. Since most of these vessels anastomose with the collateral blood supply, it is doubtful that damage to one of many supply arterioles would strangulate blood supply to the extent sufficient to cause necrosis of a tooth. Also, in cases reported here, the pulps of adjacent teeth were determined to be totally necrotic during the endodontic procedure, thus suggesting that the involved teeth had been nonvital for a prolonged period of time. Fortunately, even though these problematic cases are difficult to anticipate, they are rare and only represent 1 or 2 patients per year. Nonetheless, the implant dentist should be vigilant and carefully evaluate teeth adjacent to areas where implants are planned. Due consideration should be given to performing root-canal procedures on questionable adjacent teeth prior to instituting implant surgery.
Even though others might disagree, the authors feel that low-grade chronic infection probably existed in the vicinity of adjacent teeth in the first 3 reported cases long before implants were placed. This infection was well tolerated by patients until placement of the implants was accomplished. Once the implant surface became contaminated by the bacteria present in the bone, a more acute phase of the infection occurred resulting in clinical exacerbation and problems including draining sinus tracts (fistulas) and compromise of the implant. However, since patients had presumably built up an adequate immune defense against these particular bacteria over the years, an acute osteomyelitis did not occur in any of these cases. Thus, there was no instance of catastrophic implant failure because the infection was localized in all cases. There was no extensive bone destruction, and in each case, prompt therapeutic intervention mitigated the problem to the extent that all implants were saved.
A legion of studies reported in the literature over the years supports the fact that reactive fluoride ion is efficacious in inhibiting a variety of oral bacteria. In cases reported here, fluoride ion supplied from fluorapatite and from applied therapeutic solutions appeared at least partially effective in reducing local infection and allowing compromised dental implants to be resurrected and saved. The exact extent to which fluoride intervention alone contributes to clinical success can only be determined by controlled clinical studies, and the latter are in the planning stages. Nonetheless, 4 instances of clinical success as reported here are strongly suggestive that fluoride does in fact play a helpful role in achieving clinical osseous success in the overall treatment regimen. Further, there is no argument that fluoride use had been in place as a clinical regimen for decades, and thus far, although some would claim otherwise, has not proven toxicity issues that would contradict its use. It would therefore seem reasonable that fluoride ion released from fluoridated HA could be used in grafting infected extraction sites with OsteoGen (OsteoGen cluster, Impladent Ltd, Holliswood, NY), immediately after the surgery as an adjunctive agent to ready a site for future implant placement, and this procedure would satisfy all concerns of clinical safety. Techniques as reported here are useful in that they provide for a fluoride store thus inhibiting infection, stabilizing pH, and providing a more suitable environment for conversion of bone grafts in osseous defects to new viable bone, (as reported in Nordquist et al14).
Chronic oral infection caused by one or more of the hundreds of bacteria known to exist within the oral cavity, whether associated with an endodontically treated tooth or an asymptomatic necrotic nerve, or from periodontal disease, could well have ramifications on the success or failure of dental implants as well as potential systemic implications. These infections need to be treated quickly and aggressively. The vast majority of the implants that are otherwise subject to compromise and potential failure by low-grade infections associated with adjacent teeth are vulnerable to effects of seemingly innocent infections. Many if not all compromised implants can be saved by aggressive control of adjacent minor dental infection that may seem inconsequential but, under the superimposed stresses and insults associated with an implant, can be injurious. The fluoride ion, in any of several forms as reported here, may prove useful as an adjunct treatment measure for such local control.
Four cases of bone loss associated with undiagnosed necrotic pulp of adjacent teeth are reported. In 2 cases, bone was obliterated along fistulas (sinus tracts) that coursed between the implant and the adjacent tooth exiting at the crest. Endodontic treatment was completed on adjacent asymptomatic teeth considered as potential sources of infectious organisms that could contaminate an implant site. The latter procedures were accomplished concurrently with periapical surgery to seal teeth apices. Any apparent sinus tract was removed and the implant and tooth surfaces were treated therapeutically, employing a combination of concentrated citric acid and 4.3% sodium fluoride solutions. An augmentation procedure was completed using fluoridated resorbable microcrystalline HA OsteoGen (or FA-coated HA). All implants, though initially compromised, were successfully retained. In view of findings herein, we advise that seemingly inconsequential oral infections should be treated quickly and aggressively. It is suggested that the therapeutic use of fluoride ion in any of a variety of clinical regimens as described here, enhances the success of surgical implants previously compromised by infection. Such regimens also provide an adjunctive means for effective saving of implants that would otherwise be doomed to failure.