Abstract

With clinicians placing more dental implants, it is becoming increasingly important to maintain bone volume after tooth extraction. This article reports the results of implants placed into extraction sites grafted with particulate mineralized bone allograft (Puros). A total of 313 extraction sites were grafted with mineralized bone graft during a 36-month period. A total of 252 Tapered Screw-Vent dental implants were placed into the grafted extraction sites after a 4- to 7-month healing period. All reentries revealed a bony hard structure acceptable for osteotomy preparation. A total of 244 of these implants have been restored with fixed prosthesis and 6 with removable overdentures for a total of 250 loaded implants. A total of 6 implants failed, which required their removal (2 implants before load and 4 after loading), resulting in a 97.6% implant success rate. We conclude that mineralized human allograft placed into extraction sites is clinically useful to maintain bone volume. This material provided a bony hard structure acceptable for implant placement with good success rates.

Introduction

Growth in the dental implant industry is expected to continue from 2003 to 2007 at a compound annual rate of 9.4%.1 As clinicians increase their recommendation of dental implants after tooth extraction, it becomes necessary to retain as much bone as possible. Reports continue to show the increased benefits of bone grafting vs nongrafting.2 With the proliferation of bone grafting techniques, a search for the ideal bone replacement material has begun. In recent years, the use of gamma-radiated human mineralized allograft has increased (Puros, Tutogen Medical US Inc, Alachua, Fla).3 The purpose of this article is to present the results after 3 years of placement of dental implants into extraction sites grafted with mineralized allograft.

Whether to treat an existing failing tooth depends on many factors, including the restorability of the structure remaining, endodontic status, periodontal status, condition of adjacent teeth, traumatic forces, occlusal considerations, opposing arch, and prosthetic treatment planning. Teeth with a prognosis of less than 5 years should be considered for extraction and grafted before placement with a dental implant.4 Bone loss after extraction is often unpredictable; therefore, it is imperative that the clinician maintain as much bone as possible after tooth extraction if placement of a dental implant is anticipated.5 

The thin facial bony plate that remains after tooth extraction can often lose its blood supply, resulting in a reduced buccal lingual dimension.4 In the anterior maxilla, up to 25% of the facial bone may resorb within the first year after extraction, and in the posterior region the rate of bone loss can even be greater, with up to 50% bone loss. Limited buccal-lingual dimension after tooth extraction often results in less bone for the placement of root form implants.6 

Bone grafting materials

Bone graft materials have played an important role in regenerative dentistry for many years.2 It is common today to routinely consider maintenance of the extraction socket dimensions with some sort of bone replacement material.7 This procedure has been coined “ridge preservation.”8 The clinician essentially has 4 choices of bone graft materials: autogenous grafts, alloplasts, xenografts, and allografts.

Allografts are easily accessible graft materials available in many quantities. Allografts are tissues taken from individuals of the same species as the host.9 The main advantage of allografts is that they are readily available. The disadvantage is that patients have certain fears concerning the possible transmission of diseases from a cadaver or religious beliefs. Accredited bone banks require screening and testing before donor selection; therefore, with stringent sterilization and processing there is a 1 in 2.8 billion chance of contracting human immunodeficiency virus (HIV) from demineralized allograft, with no known occurrences reported to date.10 They provide type I collagen, which is mostly composed of the organic component of bone.

A common allograft for many years has been demineralized freeze-dried bone allograft (DFDBA). It is derived from human cadaver bone whose donors have been screened, selected, and maybe tested to be disease free of HIV and hepatitis.2 It is thoroughly processed to eliminate any diseases that might threaten the health of the recipient.11,12 

The DFDBA is ground, immersed in 100% ethanol to remove fat, frozen in nitrogen, freeze-dried, and ground to smaller particles (250–750 μm). The desiccating step allows for long-term storage and decreases antigenicity. One of the processing steps is the use of 0.6N hydrochloric acid or nitric acid, which tends to ensure its disease-free state.4 This also removes the calcium and phosphate salts (all the mineral components). After washing and dehydration, the material is either irradiated or sterilized in ethylene oxide. Ethylene oxide has been shown to have carcinogenic potential and is classified by the Occupational Safety and Health Administration (OSHA) as an occupational carcinogen and as a de minimis carcinogen, meaning that the minimum amount of the chemical set by OSHA is considered to be carcinogenic.13 

Allografts may contain bone morphogenic proteins (BMPs), which help stimulate bone growth. Assays are available to check for the quantity of BMP within bone allograft.14 The proteins that have been identified so far (BMP1 through BMP13) are considered osteoinductive compounds.2 Osteoinductive materials encourage new bone formation by acting as a signal in initiating and regulating specific tissue formation. This activity leads to a series of developmental processes that result in the differentiation of mesenchymal cells into osteoblasts. The amount of BMPs in any one allograft has shown significant variability.

Puros human allograft

According to the manufacturer, Puros is a mineralized human allograft indicated for the replacement of osseous bone structures in maxillofacial oral surgery. It promotes rapid healing and remodels completely.15 Puros is available in 2 particle sizes: 25 to 1000 μm or 1000 to 2000 μm. Tutogen Medical has performed extensive research with the Puros Accugraft, which is a 2-piece graft comprising cortical and cancellous bone to assist fusion in the lumbar spine from an anterior approach.16 Tutoplast-processed tissues have been in use for more than 25 years in more than 500 000 surgical cases without a single documented case of disease transmission.16 The authors have previously reported the histology of this material after 5-month reentry to be biologically similar to remodeling bone.17 

Materials and Methods

A total of 134 patients underwent extractions and bone grafting with mineralized allograft. Medical history for each patient was obtained in regard to cardiovascular disease, renal disease, endocrine disorders, hematologic disease, and other systemic disorders. Patients were treated if determined to have no contraindication for minor oral surgery with local anesthesia with or without conscious sedation. Both smokers and nonsmokers were included in this study. A total of 313 extraction sites were tabulated for these patients (Table).

Table 1

Data used in the statistical analysis of 313 extraction sites

Data used in the statistical analysis of 313 extraction sites
Data used in the statistical analysis of 313 extraction sites

The tooth diagnosis, prognosis, and treatment options were explained to all patients before consent for surgery. Patients were informed of the benefits of bone grafting at the time of tooth extraction to maintain as bone volume before implant placement. Patients were given informed consent forms for extraction procedures, use of human allograft products, and implant surgery.

Any hopeless tooth that required extraction was grafted, except in those patients with acute infections (pus or cellulitis) (Figure 1). Each patient underwent a complete hard and soft tissue examination, periodontal evaluation, and oral examination. Periapical radiographs, panoramic radiographs, and/or computerized tomography was performed as the clinician determined necessary (Figure 2). Diagnostic study models and photographs were obtained preoperatively as required.

Figures 1–6. Figure 1. The patient is a 66-year-old woman who presented to the office for consultation regarding the replacement of mobile lower teeth with dental implants. Figure 2. The patient exhibited class III periodontitis on tooth 29 and tooth 30, with tooth mobility. A periapical radiograph exhibited significant alveolar bone loss. Figure 3. Collagen barrier membrane (Biomend, Zimmer Dental Inc, Carlsbad, Calif) placed on the lateral aspect of the extraction socket to support the placement of mineralized bone graft material (Puros, Zimmer Dental). Figure 4. Four-month reentry into extraction sites grafted with mineralized allograft showing hard bony structure. Figure 5. Two 4.5 × 13-mm root form implants (Tapered Screw-Vent, Zimmer Dental Inc, Carlsbad, Calif) were placed as a single-stage surgery and allowed to heal unloaded for 3 months. Figure 6. Restoration with prefabricated titanium abutment fixtures and porcelain fused to metal fixed prosthesis

Figures 1–6. Figure 1. The patient is a 66-year-old woman who presented to the office for consultation regarding the replacement of mobile lower teeth with dental implants. Figure 2. The patient exhibited class III periodontitis on tooth 29 and tooth 30, with tooth mobility. A periapical radiograph exhibited significant alveolar bone loss. Figure 3. Collagen barrier membrane (Biomend, Zimmer Dental Inc, Carlsbad, Calif) placed on the lateral aspect of the extraction socket to support the placement of mineralized bone graft material (Puros, Zimmer Dental). Figure 4. Four-month reentry into extraction sites grafted with mineralized allograft showing hard bony structure. Figure 5. Two 4.5 × 13-mm root form implants (Tapered Screw-Vent, Zimmer Dental Inc, Carlsbad, Calif) were placed as a single-stage surgery and allowed to heal unloaded for 3 months. Figure 6. Restoration with prefabricated titanium abutment fixtures and porcelain fused to metal fixed prosthesis

Patients were administered preoperative antibiotic prophylaxis (amoxicillin, 2 g by mouth 1 hour preoperatively, or clindamycin, 600 mg by mouth 1 hour preoperatively).18 Patients were scheduled for extraction with local anesthesia with or without conscious sedation. Then 2% bupivacaine with 1:200 000 epinephrine or 2% lidocaine with epinephrine (Cook-Waite, Abbott Labs, North Chicago, Ill) was administered via inferior alveolar nerve, buccal nerve block, or infiltration.

Teeth were removed with an atraumatic extraction technique. Every attempt was made to extract teeth in total without a full-thickness periosteal flap to maintain the blood supply and buccal plate as best as possible. If the tooth required sectioning for extraction, all attempts were made to preserve as much bone as possible.

Defect morphologic features were evaluated at the time of extraction. Socket sites were examined for bony perforations and crestal bone height with a curette or periodontal probe. The sockets were then degranulated with a surgical curette to remove any soft tissue remnants. Bleeding points were initiated with a 1-round bur on a high-speed instrument by penetrating through the cortical bone of the extraction sockets on all walls, except the buccal wall.19 

If the buccal or lingual bony plates were missing, a barrier collagen membrane (Biomend, Zimmer Dental Inc, Carlsbad, Calif) was placed to support that wall of the extraction socket before bone grafting. The sockets were then packed with human mineralized allograft material (Puros, 0.25- to 1-mm or 1- to 2-mm particle size), depending on the size of the extraction site defect. Larger defects were packets with larger particle size.

The mineralized bone allograft was reconstituted with sterile saline solution 15 to 20 minutes before surgery or at the time of extraction. The bone graft material was gently packed to the crest of bone within the extraction socket (Figure 3). A collagen membrane (Collatape, Zimmer Dental) was placed over the extraction sockets before suturing in most large extraction sockets.19 Closure was made with 3-0 or 4-0 silk, chromic gut, or Vicryl (Ethicon Inc, Piscataway, NJ) sutures.

Immobilization of the graft was ascertained by soft diet for 1 to 2 weeks and relief of any removable prosthesis over the surgical site. A transitional removable partial denture was placed over the extraction sockets when indicated for esthetics and checked with pressure-indicating paste (Mizzy, Keystone Industries, Cherry Hill, NJ) to relieve any pressure.

Patients were given postoperative instructions, which included a soft food diet and ice for swelling. All patients were administered a prescription for 500 mg of amoxicillin 3 times daily for 2 days (or clindamycin, 150 mg, for those allergic to amoxicillin) and analgesics for 2 days (5 mg of oxycodone and 325 mg of acetaminophen every 4 hours as necessary).20 The tissue utilization record for the graft material was completed with the lot registration and forwarded to Tutogen Medical. Extraction sites were allowed to heal for 3 to 6 months, depending on the size of the defect.5 Before implant surgery the patients were given informed consent. Preoperative antibiotics (amoxicillin, 2 g by mouth 1 hour earlier, or clindamycin, 600 mg by mouth 1 hour earlier) were administered before implant surgery.18 After the patients were administrated local anesthesia (2% lidocaine with 1:100 000 epinephrine or 2% bupivacaine with 1:200 000 epinephrine, Cook Waite Abbott Labs), a full-thickness periosteal flap was elevated (Figure 4).

The extraction sockets were evaluated for hardness with a periodontal probe or surgical curette. If the probe did not penetrate the socket beyond 2 mm, the bone was considered mature. Surgical rotary instruments were used with or without osteotomes to prepare osteotomy sites for implant surgery. Tapered Screw-Vent (Zimmer Dental) implants were placed into proper tooth positions with or without a surgical stent. Either the implants were submerged with cover screws in a standard 2-stage surgery protocol or permucosal healing caps were placed in single-stage placement if at least 3 mm of existing bone was available apical to the extraction site. Some implants in the esthetic zone were immediately restored with fixed acrylic transitional prosthesis without loading. Patients were given postoperative instructions, antibiotics, and analgesics as previously described after the bone grafting procedure.20 Patients were seen 1 to 2 weeks postoperatively, and sutures were removed if necessary. Implants were allowed to heal for 3 to 6 months at which time radiographs were taken (Figure 5).21 Implants that were submerged underwent second-stage recovery surgery.

Local anesthesia was administered as described previously. A full-thickness mucoperiosteal flap was elevated, and the implant was evaluated for any crestal bone loss and/or mobility. Hand reverse torque of the implant was applied to implants before abutment placement.22 If the implant did not rotate and bone was covering the threads of the implant, it was considered a success. After permucosal abutment placement, the implants were restored with either fixed cementable porcelain fused to metal prosthesis or screw-retained bar overdentures (Figure 6).

Results

The ages of the patients ranged from 20 to 91 years. Most patients were between 51 and 60 years old. Of all the patients involved, the 41- to 50-year age group was highest for females, and the 51- to 60-year age group was highest for males (Figure 7). The grafted sockets were divided almost evenly between the maxillary and mandibular regions, with 44% occurring in the mandible and 56% occurring in the maxilla (Figure 8).

Figures 7–10. Figure 7. Analysis of patients according to sex and age groups. Figure 8. Analysis of extraction sites between maxilla and mandibular arches. Figure 9. Grafted extraction sites with implants placed and restored. Figure 10. Implant success rate vs failure rate

Figures 7–10. Figure 7. Analysis of patients according to sex and age groups. Figure 8. Analysis of extraction sites between maxilla and mandibular arches. Figure 9. Grafted extraction sites with implants placed and restored. Figure 10. Implant success rate vs failure rate

Analysis of the patients revealed a total of 313 extraction sites grafted with mineralized bone allograft during a 36-month period. Most of the patients had minimal postoperative pain and swelling after surgery. Some patients mentioned “granules” as being present in their mouths a few days postoperatively.

Postoperative follow-up visits revealed most extraction socket sites without primary intention healing over the graft site at the 1- to 2-week period. Two socket bone graft complications occurred. One patient who underwent grafting presented with an infection 5 days postoperatively. The patient's antibiotic was changed to amoxicillin-clavulanate potassium (Augmentin), 875 mg 2 times per day for 10 days, and the patient healed uneventfully. Another patient complained of pain increasing 5 days after extraction site surgery and exhibited symptoms of dry socket at 1 week postoperatively. The socket was irrigated with peroxide, and iodoform gauze (Johnson and Johnson Inc, New Brunswick, NJ) with dry socket paste was placed for 3 days. This patient also recovered without complication. These 2 patients with graft failure did not have implants placed and were not included in the implant group.

Following a 3- to 6-month healing period, grafted sites needed for implant surgical sites placement as determined by presurgical prosthetic treatment planning were reentered via a full-thickness mucoperiosteal flap. The bone grafted extraction sites all appeared to be bony hard in consistency. The sites were not penetrable with a surgical curettage for more than 1 to 2 mm. Tapered Screw-Vent implants were placed into 252 extraction sites and submerged, left exposed with a healing collar, or immediately restored. Of those 252 implants placed, 2 were not uncovered to date.

The remaining 250 implants were either uncovered or restored and loaded. Loading with either a fixed prosthetic restoration or bar overdenture was performed during a 3- to 6-month period (Figure 9). A total of 6 implants were considered failures. Two of these failed implants occurred in a single patient and were removed after 3 months because the patient was experiencing pain. Within a 4-month period, 4 more implants failed (had mobility and/or radiolucency) in 4 other patients and were removed. The remaining 244 implants showed good soft tissue anatomy, which was clinically acceptable. Radiograph examination of all remaining implants did not show any peri-implant radiolucency. The combined total of implant failures amounted to 6. A total failure rate was concluded to be 2.4%. A total implant success rate of 97.6% was established (Figure 10).

Discussion

This report presents the statistical analysis of 313 extraction sites grafted with human mineralized allograft (Puros). A total of 252 implants were placed into these extraction sites 3 to 6 months later. Of these 252 implants, 250 were either single stage placed with a healing cap, immediately loaded, or exposed in a stage 2 surgical uncovering 3 to 6 months after placement. The purpose of this study was to evaluate the survival rate of implants placed into sockets grafted with mineralized allograft.

Patients often need to be evaluated for both the short- and long-term prognosis for a tooth. The clinician has a responsibility to recommend the best long-term treatment available for the patient after extraction, which is often a dental implant. With the increased recommendation of dental implants as a tooth replacement, it becomes important for the dentist to consider ridge preservation at the time of tooth extraction.8 

The periosteum is an important structure vital to alveolar bone formation.4 Whether implant placement is delayed or immediate, careful atraumatic extraction techniques and maintenance of the periosteum help to preserve alveolar bone.

Unpredictable bone loss can occur after tooth extraction, particularly if there is an existing bony defect or radiolucency present.5 Today an abundant amount of bone replacement graft material is available to the clinician.2 Although alloplastic materials are plentiful and inexpensive, concerns arise regarding their predictability in achieving bone replacement before implant placement. Often a fibrous connective tissue encapsulation of the residual graft particles occurs, which can delay or complicate dental implant placement.23 The use of human allograft has long been established as a good alternative to patient autogenous grafting, since it avoids the need for bone grafting from the other sites.2 

Piattelli et al24 showed the main differences between freeze-dried bone allograft (FDBA) and DFDBA. In FDBA the resorption process is scarce and cells with acid phosphatase are not found, whereas with DFDBA resorption is present and cells are positive for acid phosphatase. In FDBA all osteocytic lacunae are filled by osteocytes, and in some areas Haversion systems with a capillary center are found. In DFDBA the osteocytic lacunae are mainly empty.24 

Puros is a mineralized human allograft with an excellent history of efficacy and safety. Mineralized human allograft has the advantage of providing both the BMP and minerals necessary to achieve osteoinductive properties. Use of a bone augmentation material with mineral content instead of DMFBA is often preferable, especially when lateral ridge augmentation is required before dental implant placement.25 

Puros is obtained from human cancellous bone. The material is processed by 27 washes of various fluids and solutions that remove fats, cellular material, and noncollagenous proteins. Collagen is maintained, which provides a bone matrix similar to natural bone. These washes deactivate and destroy any remaining proteins that may be pathogenic but preserve BMPs, which contribute to osseoinduction. Delipidization appears to be an essential technique in the management of bone banks, especially when radiation is used. Studies indicate cytotoxic compound formation within the graft in the presence of lipids.11 Some authors have shown that higher irradiation (3 to 5 Mrad) of allograft enhanced bone induction in rats.26 The use of irradiation doses above 2.5 Mrad is controversial, since high doses of irradiation can be destructive to bone formation.27 Puros receives low-dose gamma irradiation (17.8 kGy), which inactivates all remaining viruses but preserves protein structure (Christopher Schopt, biologist, head of processing, Tutogen Medical, Neunkirchen, Germany, written comm-unication, October 23, 2002).

Delayed vs immediate implant placement is a clinical decision that the implant dentist must face. The standard regimen for root form implant placement as described by Branemark et al28 has been to extract a tooth and allow the socket to heal for a period of up to 6 months before reentry for implant placement. Recently, literature has shown that implants can be placed immediately into extraction sites and either restored (loaded) or submerged.29–31 

To place an implant at the time of extraction, a few prerequisites exist. Ideally, the site should not be infected and the socket should simulate the size of the implant as close as possible. Having the implant engage in existing bone several millimeters past the apex of the extraction site for immediate fixation has been recommended.32 The prerequisites for immediate implant placement do not always occur. Concern arises when a thin facial bony plate of the tooth socket site is resorbed because of periodontal bone loss, infection, or fracture at the time of extraction. Grafting the extraction site and delaying the placement of a dental implant allow for maturation of the extraction site before insertion.

Some authors have advocated the immediate placement of implants without the use of graft material.33 This procedure is viable for patients who present with sufficient bone at the time of extraction to support implant placement. This report demonstrated a reliable method for regenerating bone before implant surgical placement, whether or not sufficient bone is available at the time of tooth extraction. The results obtained in this study show that delayed placement of dental implants after grafting allow for maturation of the extraction site with good survival rates of implants placed into these grafted sites.34 

The authors of this report have placed particulate mineralized bone allograft (Puros) into the extraction sites of more than 134 patients. Extraction sites with acute infections (exudate, acute pain, or cellulitis) were excluded from graft placement at the time of extraction. Relatively few complications besides swelling and postoperative pain occurred.

The mineralized allograft was easy to use after extraction and resulted in normal healing of the soft and hard tissues with the exception of 1 infection and 1 dry socket in 134 patients. Most extraction sites were allowed to heal for a period of 3 to 6 months before reentry for dental implant placement. After healing, the graft material appears clinically to form a dense bony structure within the extraction site, which allows the surgeon to place implants in a conventional manner.

On reentry for dental implant surgery, the material generally appeared hard and resistant to osteotomy preparation. The authors' previous human histologic analysis, at the light microscopic level, revealed nonvital spicules of mature calcified bone that had a highly organized matrix surrounded by viable noncalcified immature bone matrix or osteoid.17 

This material was clinically useful to maintain bone volume for implant placement after extraction. The extraction graft sites were sufficiently dense enough to withstand an osteotomy drilling procedure in a period of 3 to 6 months. The tapered-shaped root form implants placed on these patients were useful for fixation in immature socket grafts, possibly giving greater initial implant stability.35,36 

A total of 313 extraction sites were grafted with mineralized bone graft during a 36-month period. A total of 252 Tapered Screw-Vent dental implants (Zimmer Dental) were placed into the grafted extraction sites after a 4- to 7-month healing period. A total of 244 of these implants have been restored with fixed prosthesis and 6 with removable overdentures for a total of 250 loaded implants. A total of 6 implants failed, which required their removal (2 implants before load and 4 after loading), resulting in a 97.6% implant success rate.

The implants placed in this study ranged from 6 to 32 months after loading observation. Although this is a short time frame for statistical survival rate follow-up, the graft material appears to have been beneficial in maintaining bone width before implant placement.5 

Conclusion

With clinicians placing more dental implants, it is becoming more important to maintain bone volume after tooth extraction. Given the abundant scientific literature of bone grafting materials, clinicians who perform oral surgery are often recommending ridge preservation to their patients before extraction. There are many different bone grafting materials available to the dentist.

Mineralized bone allograft (Puros) is an easily procured material. This article presents a 3-year analysis of implants placed into extraction sites grafted with this allograft. A total of 252 Tapered Screw-Vent implants were placed into this graft material and 250 were exposed or occlusally loaded. A total of 6 implants failed, which required removal (2 implants before loading and 4 after loading) and resulted in a 97.6% success rate. The authors have previously presented study results that exhibited new osteoid bone formation within a human extraction socket grafted with mineralized cancellous allograft.17 

We conclude that mineralized human allograft placement into extraction sites is clinically useful to maintain bone volume and provide a bony hard structure that facilitates successful implant placement. Further long-term controlled studies are recommended to determine the efficacy and safety of this material.

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Table 1

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Author notes

John C. Minichetti, DMD, is in private practice in Englewood, NJ. He is on the attending staff at Englewood Hospital. Address correspondence to Dr Minichetti at 70 Grand Avenue, Englewood, NJ 07631 (Dminichett@aol.com).

Joseph C. D'Amore, DDS, is in private practice in Englewood, NJ.

Anna Y. J. Hong, DDS, is in private practice in Englewood, NJ, and is a clinical instructor at Bergen County Community College in New Jersey.