Maxillary Sinus Augmentation

Gonshor et al INTRODUCTION with or without autogenous bone. Hising et al16 showed much higher implant survival rates when A lack of vertical height in the posterior maxilla an ABBM was used alone (92.2%), than when it often precludes implant placement. The loss of was used together with autogenous bone (77.2%). maxillary molars often results in very large reduc- tions of bone volume in both horizontal and ver- The present article highlights the use of two tical directions, precluding implant placement.1 ABBMs- NuOss™ (ACE Surgical, Brockton, Mass, In addition to this quantitative loss there is also USA) and Bio-Oss® (Geistlich, Wolhusen, Switzer- the factor of bone quality affecting the implant land) - in an ongoing clinical human sinus augmen- anchorage. Often there is little or no corti- tation project. Histologic studies have shown that cal bone in the posterior maxilla, as well as very the ABBMs have bone-conductive properties17, 18 low density cancellous bone. Both of these fac- and that they have prolonged resorption times.19 tors decrease the chance of achieving good primary stability during implant placement.2 MATERIALS AND METHODS Greater bone volume and height can be Materials achieved by augmentation of the maxillary The inorganic component of bone is comprised sinus floor, so as to provide a sufficient vol- of calcium-based minerals of apatite structure, ume of bone for mechanical support. The tech- mainly of carbonate apatite, containing small nique for antral augmentation was developed amounts of magnesium, sodium, potassium, by Tatum in the 1970s and reported in 1986,3 chloride, etc. It has been demonstrated that the but the first clinical results were presented organic part of bone can be removed without sig- by Boyne and James.4 Apart from the tech- nificantly altering the native structure of the bone nique itself, one of the key features in the suc- mineral.20 Methods have been developed that cess of the procedure involves the selection can produce this anorganic bone mineral from of the appropriate augmenting graft material.5 a bovine source, while maintaining the struc- ture of the mineral similar to that in native bone. Autogenous bone has long been considered Essentially the method consists of a chemical the gold standard in grafting procedures,6 but is extraction process and heat treatment to remove often limited by the morbidity of a second surgi- the organic components of the bone resulting cal site and the frequent inadequate amounts in an anorganic bovine bone mineral, a natural of graft obtained.7 This has led to the use of a calcium phosphate salt in a carbonate apatite myriad of substitutes as grafting material, includ- structure. In the present study the ABBM gran- ing allografts,8 coralline hydroxylapatite,9 synthetic ules were cancellous, in the 250 to 1000µ size. calcium phosphates,10 anorganic bovine bone,11-13 or a combination of these materials.14 In particu- Patients lar, there has been considerable clinical evidence This multicenter study took place from May, that anorganic bovine bone mineral (ABBM) gives 2005 to February, 2007. Twelve patients (1 very similar results to autogenous bone as a sinus female, 11 males), with a mean age of 52 grafting material.15 Froum et al11 showed similar years (range 41 to 70) took part in the study. implant survival rates when an ABBM was used 50 Vol. 1, No. 8 November 2009

Gonshor et al Figure 1a: Cross sectional CBCT image after grafting. Figure 1c: Cross sectional CBCT image after case completion. Figure 1b: Panoramic CBCT image after grafting. Figure 1d: Panoramic CBCT image after case completion. There were 4 totally and 8 partially edentulous ing, diabetes or autoimmune disease, abscess patients, all with bilateral posterior maxillary with soft-tissue swelling, oral bisphospho- bone loss and sinus pneumatization, preclud- nates, and active sinus disease or sinus pathol- ing the placement of implants. This created 22 ogy. Each patient was given information about maxillary sinus augmentations. The inclusion the study and gave written and oral consent. criterion was that the residual alveolar bone be no higher than 5mm, as determined by Com- Surgical Procedure puterized or Cone Bean Scans (figures 1a,1b). All of the patients underwent the sinus floor aug- The average residual bone height was 3.8mm mentation under local anesthetic. The surgical (±0.4mm). The exclusion criteria were smok- procedure has been described elsewhere.4 An The Journal of Implant & Advanced Clinical Dentistry 51

Gonshor et al incision was made in a slightly palatal portion of the residual ridge crest while vertical releasing Figure 2: ABBM placement into maxillary sinus. incisions were made both anteriorly and posteri- orly. The creation of a superiorly-lifted mucope- Figure 3: Histologic core sample. riosteal flap permitted visualization of the lateral maxillary bone with a view of the buccal sinus 52 Vol. 1, No. 8 November 2009 wall. Using diamond-tipped burs, a window was created in the lateral maxillary buccal wall, revealing the Schneiderian membrane. The lat- ter was separated from the underlying bone so as to create a submembrane cavity into which the graft material was placed. There was no infracturing of the buccal wall. In each case, the treatment was to augment the sinuses with the ABBM - NuOss™ on one side and Bio-Oss® on the other (figure 2). In one of the patients platelet rich plasma (PRP) was mixed with the ABBM’s. Implants were placed at a later date. In all cases, after the graft material was placed, the window opening was covered with a long acting resorbable collagen membrane (RCM-6, ACE Surgical, Brockton, Mass, USA). Closure was performed with 3.0 Vicryl® sutures (John- son and Johnson, Langhorne, PA, USA) in both continuous and horizontal-mattress fashion. Core Biopsies After an average of 6.4 months of healing, cores were taken for histologic and histo- morphometric analysis (figure 3) and dental implants were placed. Biopsy cores were taken with trephines of 2.7 mm internal diam- eter (3.5 mm external diameter). The Biop- sies were left within the trephine and placed in 10% neutral buffered formalin for fixation. Histological Preparation Histological preparations were performed at

Gonshor et al Figure 4a: High resolution histology of bone formation in Figure 4b: High resolution histology of bone formation in graft with Bio-Oss® graft with NuOss™ the Department of Oral Pathology, Yonsei Uni- The cores were digitized at the same magnifi- versity College of Dentistry, Seoul, Korea and cation using a Leica DMR HC and a Jenoptic at the Periodontal Bone Center, McGill Univer- ProgRes C14 Digital camera. Histomorpho- sity, Montreal, Quebec, Canada. Upon receipt, metric measurements were completed using specimens were dehydrated with a graded ser- Bioquant Nova Prime Bone Morphometry, ver- ies of alcohols for 9 days. The specimens were sion 6.50.10 (Bioquant Image Analysis Corp. then infiltrated with a light-curing embedding - Nashville, Tenn, USA). Parameters evaluated resin. After a further 20 days, the specimens were the total area of the core, the percentage were embedded and polymerized by 450 nm of new bone formation, and the percentage of light. The specimens were then prepared by the residual graft material. The remainder of the cutting/grinding method of Donath21 and Roh- area was considered as being soft-tissue, void rer.22 The cores were then polished to a thick- or osteoid. The primary slide evaluated for each ness of 45-65 µm, followed by a final polish with specimen was from the most central region of 0.3 micron alumina polishing paste. The slides the obtained core. No comparison was made were stained with Hematoxylin-Eosin (H&E) and between the apical and coronal sections. coverslipped for histologic analysis by means of bright field and polarized microscopic evaluation. RESULTS Histomorphometry Histology Following non-decalcified histologic prepara- The histologic results are represented in figures tion, the cores were evaluated morphometrically 4a and b. In all cases, even those that had an at McGill University, Montreal, Quebec, Canada. 8-10 month healing period between grafting and core removal, residual particles of ABBM The Journal of Implant & Advanced Clinical Dentistry 53

Gonshor et al were still clearly visible. For both Bio-Oss® and factor affecting the percentage of new bone NuOss™ there was significant bone growth in formation. It would seem that individual healing intimate contact with the grafted particles. The response, rather than the time the bone mate- bone was mostly of the woven variety, but there rial was in place, had the greatest effect on was also ample evidence of more mature lamel- the ABBM integration. There were also large lar bone formation. The newly-formed bone variations in bone healing around the ABBM’s could be easily distinguished from the grafted regardless of age and sex of the subjects. ABBM as the bovine bone mineral exhibited empty lacunae, with no osteocytic nuclei and DISCUSSION no lamellar layering. This was contrasted by the new viable bone with osteocyte nuclei. In addi- Bio-Oss and NuOss are both sterile anorganic tion, there was bridging of new bone between bovine bone materials with porosity in the range particles - a cardinal sign of active bone growth. of 75-80%. The inner macropores of ABBM’s The ABBM particles were often thick and jag- are similar to natural cancellous bone.23 No ged-edged as opposed to the new viable bone B-cell or T-cell inflammatory responses have which exhibit long lamellae with indefinite bound- been reported with the use of the ABBM.24 Bio- aries. There was also evidence of connective Oss has been shown to be biocompatible with tissue distributed amongst the graft particles oral osseous tissue, fulfilling a major require- and new bone trabeculae, containing blood ves- ment of an osteoconductive material. The deg- sels, collagenous fibers and fibroblasts. There radation of these materials has been studied were no signs of inflammation. Although there extensively. When ABBM’s were first used, they were few signs of active osteoclasts, the new were considered as bioresorbable materials that bone ingrowth was evidence of slow replace- would be replaced by autogenous bone over ment of the grafted particles by new viable bone. time. More recent studies have shown histologi- cal evidence that ABBMs are not resorbed with Histomorphometry time. Hallman et al,19 working with human sub- The histomorphometric analysis revealed jects, demonstrated that residual ABBM content remarkably similar results for both ABBM’s. did not decrease from 6 months to 3 years after The average percentage of new vital bone was grafting. Other authors have confirmed this slow 33%, with a large standard deviation in the resorption, with very few resorption lacunae,25 24-29% range. The ABBM amounts were also or almost no resorption at all.26 Working with close in value, with an average of 24% (±11) Bio-Oss, Avera et al27 showed particles pres- for NuOss™ and 29% (± 17) for Bio-Oss®. ent after 44 months, and Piattelli et al confirmed The amount of soft tissue was also similar, with particle presence after 4 years.18 Instead, it 39% (±21) for NuOss™ and 43% (± 14) for appears that the graft particles become embed- Bio-Oss®. Notwithstanding a period of 5 to10 ded in the newly generated lamellar bone, creat- months before removing the bone cores, the ing a more radiopaque, dense bone than would duration of waiting time was not a significant be the case if the ABBM had resorbed.28 In fact, it has been suggested that the resistance 54 Vol. 1, No. 8 November 2009

Gonshor et al of ABBM’s to resorption may help in maintain- rate when only 3mm of residual bone remained. ing initial stability in the augmented areas.11,29 The histomorphometric analysis showed that As has been described elsewhere,13,30 in the amount of new bone formation for the two this study newly generated bone was seen in bone materials was about 33%, with the non- intimate contact with the ABBM particles. The vital particle percentage around 26%. These length of wait from grafting to core samples results are close to the findings of other stud- was not identifiable as a factor in the percent- ies with using autogenous bone alone as ages of new bone creation. It may be assumed a graft material in sinus augmentation26 or that the variation in percentage is more a factor in defects around dental implants.33 All of of individual healing and regeneration response. these studies, as well as the present results, The percentages were also not related to indicate that the use of this bovine mate- patient age or sex. The amount of vital bone rial will lead to predictable bone formation. is nevertheless substantial for that post-graft time period, rising to above 30%. In addition CONCLUSION there is still a high percentage of non-vital bone remaining. This is consistent with the general This study showed the osteoconductive prop- fact that these bovine minerals resorb slowly.25 erties of both NuOss™ and BioOss® and con- Lastly, the remaining marrow and fibrous tissue firms their effectiveness as natural bone grafting showed no signs of inflammatory response or substitutes. The clinical findings revealed giant cell invasion. This highlights the fact that significant bone formation during the period both of these materials are well accepted by the of the post grafting study. The results high- recipient. There was no significant difference in light and confirm the fact that grafting materi- percentages of vital or non-vital bone between als from a bovine source will produce reliable the case where PRP was added and the remain- bone foundations for implant placement. ing cases in the study. This is not unexpected, since the effect of PRP is most pronounced Correspondence: when it is associated with autogenous tissue, Dr Aron Gonshor which contains living cells. Its effect on non-vital 4980 Glencairn Ave grafts such as the ABBM’s is not significant.31 Montreal, Quebec Canada, H3W 2B2 The inclusion criteria used for sinus floor Phone: 514 941 4502 augmentation are important determinants of the email: [email protected] eventual clinical result. It is likely that with the decreasing amount of residual bone below the sinus floor, the role played by the grafted bone in achieving implant support becomes increas- ingly important. In that regard, Jensen and Greer32 showed a 100% survival rate when the residual bone was 7mm and a 29% survival The Journal of Implant & Advanced Clinical Dentistry 55

Gonshor et al Disclosure 13. Yildirim M, Spiekermann H, Biesterfeld S, 23. Berglundh T, Lindhe J. Healing around The authors report no conflicts of interest with Edelhoff D. Maxillary sinus augmentation implants placed in bone defects treated with anything mentioned in this article. using xenogenic bone substitute material Bio-Oss: An experimental study in the dog. Bio-Oss in combination with venous Clin Oral Implants Res 1997;8:117-124. References blood. A histologic and histomorphometric 1. Watzek G, Ulm CW, Haas R (eds). The study in humans. Clin Oral Implants Res 24. McAllister B, Margolin M, Cogan A, Taylor 2000;11:217-219. M, Wollins J. Residual lateral wall defects Sinus Bone Graft. Anatomic and physiologic following sinus grafting with recombinant fundamentals of sinus floor augmentation. 14. Moy PK, Lundgren S, Holmes RE. Maxillary human osteogenic protein-1 or Bio-Oss in the Chicago: Quintessence, 1999. sinus augmentation: Histomorphometric chimpanzee. Int J Periodontics Restorative analysis of graft materials for maxillary sinus Dent 1998;18:227-239. 2. Misch CE. Effect on treatment plans, surgical floor augmentation. J Oral Maxillofac Surg approach, healing, and progressive bone 1993; 51: 857-862 25. Storgard-Jensen S, Aaboe M, Pinholt E, loading. Int J Oral Implantol 1990; 6: 23-31. Hjorting-Hansen E, Melsen F, Ruyter I. Tissue 15. Hallman M, Sennerby L, Lundgren S. A reaction and material characteristics of 3. Tatum OH. Maxillary and sinus implant Clinical and Histologic Evaluation of Implant four bone substitutes. Int J Oral Maxillofac reconstructions. Dental Clin North Am 1986; Integration in the Posterior Maxilla After Sinus Implants 1996;11:55-66. 30: 207-229. Floor Augmentation with Autogenous Bone, Bovine Hydroxyapatite, or a 20:80 Mixture. Int 26. Valentini P, Abensur D, Densari D, Graziani 4. Boyne PJ, James RA. Grafting of the maxillary J Oral Maxillofac Implants 2002;17:635-643. JN, Hammerle C. Histological evaluation of sinus floor with autogenous marrow and bone. Bio-Oss in a 2-stage sinus floor elevation and J Oral Surg 1980; 38(8): 613-616. 16. Hising P, Bolin A, Branting C. Reconstruction implantation procedure. A human case report. of severely resorbed alveolar crests with Clin Oral Implants Res 1998; 9: 59-64. 5. Jensen OT, Shulman LB, Block MS, Iacono VJ. dental implants using a bovine bone mineral Report of the Sinus Consensus Conference of for augmentation. Int J Oral Maxillofac 27. Avera SP, Stampley WA, McAllister BS. 1996. Int J Oral Maxillofac Implants 1998;13 Implants 2001;16:90-97. Histologic and clinical observations of Suppl:11-45. resorbable and nonresorbable barrier 17. Hallman M, Lundgren S, Sennerby S. membranes used in maxillary sinus graft 6. van den Bergh JPA, ten Bruggenkate CM, Histological analysis of clinical biopsies containment. Int J Oral Maxillofac Implants Krekeler G, Tuinzing DB. Sinus floor elevation taken 6 months and 3 years after maxillary 1997;12:88-94. and grafting with autogenous iliac crest bone. sinus floor augmentation with 80% bovine Clin Oral Implants Res 1998;9:429-435. hydroxyapatite and 20% autogenous bone 28. Schlegel A, Donath K. Bio-Oss: A resorbable mixed with fibrin glue. Clin Implant Dent Relat bone substitute? J Long Term Eff Med 7. Kalk WW, Raghoebar GM, Jansma J, Boering Res 2001;2:87-96. Implants 1998;8:201-209. G. Morbidity from iliac crest bone harvesting. J Oral Maxillofac Surg 1996;54:1424-1429. 18. Piattelli M, Favero GA, Scarano A, Orsini G, 29. Scarano A, G. P, Piattelli M, Piattelli A. Piattelli A. Bone reactions to anorganic bovine Osseointegration in a Sinus Augmented With 8. Nishibori M, Betts NJ, H. S, Listgarten MA. bone (Bio-Oss) used in sinus augmentation Bovine Porous Bone Mineral: Histological Short term healing of autogenous and allogenic procedures: A histologic long-term report Results in an Implant Retrieved 4 Years bone grafts after sinus augmentation: A report of 20 cases in humans. Int J Oral Maxillofac After Insertion. A Case Report. J Periodontol of 2 cases. J Periodont 1994;65:958-966. Implants 1999;14:835-840. 2004;75:1161-1166. 9. Smiler DG, Holmes RE. Sinus lift procedure 19. Hallman M, Cederlund A, Lindskog S, S. L, 30. Skoglund A, Hising P, Young C. Clinical using porous hydroxyapatite: A preliminary Sennerby L. A clinical histologic study of and histologic examination in humans of clinical report. J Oral Implantol 1987;13:239- bovine hydroxyapatite in combination with the osseous response to implanted natural 253. autogenous bone and fibrin glue for maxillary bone mineral. Int J Oral Maxillofac Implants sinus floor augmentation. Results after 6-8 1997;12:194-199. 10. Zijderveld SA, Zerbo IR, van den Bergh months of healing. Clin Oral Implants Res JPA, Schulten EAJM, ten Bruggenkate CM. 2001;12:135-143. 31. Froum S, Wallace S, Tarnow D, Cho S. Effect Maxillary sinus floor augmentation using a of Platelet-Rich Plasma on Bone Growth and beta-tricalcium phosphate (Cerasorb) alone 20. Johnson G, Mucalo M, Lorier M. The Osseointegration in Human Maxillary Sinus compared to autogenous bone grafts. Int J processing and characterization of animal- Grafts: Three Bilateral Case Reports. Int J Oral Maxillofac Implants 2005;20:432-440. derived bone to yield materials with Periodontics Restorative Dent 2002;22:45- biomedical applications: part 1: modifiable 53. 11. Froum SJ, Tarnow DP, Wallace SS, Rohrer porous implants from bovine condyle MD, Cho SC. Sinus floor elevation using cancellous bone and characterization of bone 32. Jensen O, Greer R, . (eds). Immediate anorganic bovine bone matrix (OsteoGraf/N) materials as a function of processing. J Mater placing of osseointegrating implants into the with and without autogenous bone: a Sci Mater Med 2000;11:427-441. maxillary sinus augmented with mineralized clinical, histologic, radiographic, and cancellous allograft and Gore-Tex: Second- histomorphometric analysis-Part 2 of an 21. Donath K, Breuner G. A method for the stage surgical and histological findings. ongoing prospective study. Int J Periodontics study of undecalcified bones and teeth Chicago: Quintessence 1992. Restorative Dent 1998;18:528-543. with attached soft tissues. The Sage-Schliff (sawing and grinding) technique. J Oral 33. Hammerle C, Chiantella G, Karring T, Lang 12. Froum SJ, Wallace SS, Cho S-C, Elian N, Pathol 1982;11:318-326. N. The effect of a deproteinized bovine bone Tarnow DP. Histomorphometric comparison of mineral on bone regeneration around titanium a biphasic bone ceramic to anorganic bovine 22. Rohrer M, Schubert C. The cutting-grinding dental implants. Clin Oral Implants Res bone for sinus augmentation: 6 to 8-month technique for histologic preparation of 1998;9:151-162. postsurgical assessment of vital bone undecalcified bone and bone-anchored formation. A pilot study. Int J Periodontics implants. Improvements in instrumentation Restorative Dent 2008;28:273-281. and procedures. Oral Surg Oral Med Oral Pathol 1992;74:73-78. 56 Vol. 1, No. 8 November 2009

Gonshor et al

Does your bone grafting material measure up? Improvements in clinical and radiographic parameters in the GEM 21S® pivotal trial compare favorably with or exceed, documented outcomes for other regenerative therapies in studies examining defects with similar baseline characteristics.1,2,3,4 Radiographic Percent Bone Fill (BF%) Radiographic Linear Bone Growth (LBG) Clinical Attachment Level (CAL) Gain 60 3.0 4.0 57 3.7 40 2.6 3.0 2.0 2.7* Mean % BF 2.0 Mean LBG (mm) CAL Gain (mm) 0 20 1.0 1.1* GEM 21S® Enamel Matrix 14* Derivative (EMD) 0 0 GEM 21S® Enamel Matrix GEM 21S® Enamel Matrix Derivative (EMD) Derivative (EMD) *EMD results at 8 months, GEM 21S® results at 6 months To learn more, please visit us online at www.osteohealth.com or call 1-800-874-2334 View prescribing information: www.osteohealth.com/documents/52.pdf IMPORTANT SAFETY INFORMATION GEM 21S® Growth-factor Enhanced Matrix is intended for use by clinicians familiar with periodontal surgical grafting techniques. It should not be used in the presence of untreated acute infections or malignant neoplasm(s) at the surgical site, where intra-operative soft tissue coverage is not possible, where bone grafting is not advis- able or in patients with a known hypersensitivity to one of its components. It must not be injected systemically. The safety and effectiveness of GEM 21S® has not been established in other non-periodontal bony locations, in patients less than 18 years old, in pregnant or nursing women, in patients with frequent/excessive tobacco use (e.g. smoking more than one pack per day) and in patients with Class III furcations or with teeth exhibiting mobility greater than Grade II. In a 180 patient clinical trial, there were no serious adverse events related to GEM 21S®; adverse events that occurred were considered normal sequelae following any periodontal surgical procedure (swell- ing, pain). For full prescribing information, go to www.osteohealth.com or call 1-800-874-2334 and a copy will be sent to you. References: 1. Nevins M, Giannobile WV, McGuire MK, Mellonig JT, McAllister BS, Murphy KS, McClain PK, Nevins ML, Paquette DW, Han TJ, Reddy MS, Lavin PT, Genco RJ, Lynch SE. Platelet Derived Growth Factor (rhPDGF-BB) Stimulates Bone Fill and Rate of Attachment Level Gain. Results of a Large Multicenter Randomized Controlled Trial. J Periodontol 2005; 76: 2205-2215. 2. Heijl L, Heden G, Svardstrom G, Ostgren. Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony periodontal defects. J Clin Periodontol 1997; 24: 705-714. 3. Zetterstrom O, Andersson C, Driksson L, et al. Clinical safety of enamel matrix derivative (EMDOGAIN) in the treatment of periodontol defects. J Clin Periodontol 1997; 24: 697-704. 4. See full prescribing infromation for more detail. Emdogain® is a registered trademark of BioVentures BV Corporation. ©COPYRIGHT Osteohealth Company 2008. All rights reserved. OHD235e Rev. 9/2009.

Preservation of Buccal Bone Plate after Novaes et al Immediate Implant Placement/Function with the Flapless Approach: A Case Report Arthur B. Novaes Jr., DDS, MScD, DSc1 2 Abstract 3 Background: Immediate placement of implant was conducted 12 months later in order to into an extraction socket provides both patient verify the status of the cervical buccal plate, as and the clinician with the advantages of sig- well as the regression of the periapical lesion. nificantly decreasing treatment time by mini- mizing the surgical stages and helping to Results: The 12-month post-opera- maximize the esthetic outcome by prevent- tive CT shows the complete healing of ing alveolar ridge and gingival resorption. the periapical lesion in addition to pres- ervation of the cervical buccal plate. Methods: An immediate implant was placed through flapless approach in order to replace Conclusion: The benefit of the combina- the hopeless right central incisor due to an tion of immediate implant placement/function extensive periapical lesion. After implant place- and flapless approach can make possible the ment, a minimally functional fixed provisional maintenance of cervical buccal bone plate. restoration was inserted. A CT scan analysis KEY WORDS: Dental implants, immediate function/loading, computed tomography, dental esthetics 1. Professor & Chairman of Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. 2. Graduate Student of Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. 3. Assistant Professor of Prosthodontics, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. The Journal of Implant & Advanced Clinical Dentistry 59

Novaes et al INTRODUCTION Figure 1: Periapical radiograph of the right central incisor. One of the most challenging procedures in placement often results in two major problems: implant dentistry is the replacement of teeth in reduction of primary initial stability and soft tis- the esthetic zone. Today, the development of sue ingrowth during the healing period.14 Most an esthetic restoration that matches the adja- often, the initial stability can be preserved by plac- cent natural dentition has become the focus ing an implant that is longer that the extracted of attention in implant dentistry. Evaluation of root or wider in diameter in the apical third. The the periodontal tissues is critical to achieve an maintenance of the existing gingival architecture esthetic outcome as the alveolar bone has a is essential in achieving an esthetic result, and tendency to resorb following tooth loss and the for this purpose, the flapless approach may be soft tissues generally shrink.1-4 This is especially indicated. Therefore, the prevention of soft tis- obvious in the anterior region where thin buc- sue ingrowth and/or gingival recession around cal bone plates are often present.5,6 This loss of the implant is a prerequisite in esthetically driven bone and soft tissue lead to esthetic issues that implant dentistry. Recent investigations have may compromise the restorative outcomes.7-9 reported high survival rates of immediately pro- Observations on cadaver specimens indicated visionalized single-tooth implants in the maxilla that following tooth loss in the maxilla, the height of the ridge reduces and the crest shifted pala- tally.10 Tylman & Tylman stated that following the removal of teeth, the buccal alveolar bone plate resorbed much faster than the palatal plate.11 A paradigm shift from the restoration-driven implant placement to a tissue-related, esthetically driven approach has recently favored the concept of immediately implants placed into extraction sites.12,13 This concept helps to preserve soft and hard tissue architecture and therefore reduces the potential risk for the resorptive processes at the alveolar ridge. A goal of current research in implantology is to improve patient satisfaction and the esthetics of restored dental implants. Imme- diate placement of an implant into an extraction socket provides both patient and clinician with the advantages of significantly decreasing treat- ment time by minimizing the surgical stages and helping to maximize the esthetic outcomes by reducing alveolar ridge and gingival resorption. However, immediate post-extraction implant 60 Vol. 1, No. 8 November 2009

Novaes et al Figure 2: Cross-sectional tomography image showing Figure 3: Negative image of gure 2 . an apical hypodense area and the cervical position of the buccal bone plate. CASE DESCRIPTION AND RESULTS after a follow-up of 12 to 18 months.15-17 This approach guides the healing and the matura- The patient was diagnosed through radiographic tion of the soft tissues, favoring formation of the examination with a hopeless maxillary right central papillae through the orientation of the emergency incisor (figure 1) due to an extensive apical lesion profile shaped by the temporary prosthesis. and long post and core restoration. The treatment Moreover, the loss of bone after tooth extraction, plan was to replace the tooth with an implant- followed by additional bone loss in the first year supported crown using the flapless approach and after implant loading, could severely modify the immediate provisionalization. The patient signed an architecture of hard and soft tissues, compromis- informed consent form and treatment was initiated. ing the final esthetic outcome of implant therapy. At the first periodontal visit, the compro- The aim of this case report is to demonstrate mised periodontal sites were detected, com- through computed tomography (CT) scan analy- prehensive oral hygiene and full-mouth scaling sis, the possibility of maintenance of the cervical and root planning was performed. Following the buccal bone plate after immediate implant place- achievement of satisfactory levels of plaque con- ment followed by immediate function protocol. The Journal of Implant & Advanced Clinical Dentistry 61

Novaes et al Figure 4: Flapless approach. Implant placed 1-1.5mm Figure 5: Full-thickness ap elevated . away from the buccal bone wall. that the third dose was taken one hour before the trol the patient was scheduled for the surgery. surgery. A flapless surgery was carried out with Based on the information gained from initial atraumatic extraction of the hopeless tooth using a periotome. After the root was mobilized, it was radiographs and bone mapping, a diagnostic wax- carefully removed with forceps in a manner that up was made on articulated casts. The final posi- minimized trauma to soft tissue and alveolar bone. tion of the gingival margins and the apicocoronal The extraction socket was thoroughly debrided, dimensions of the crown were established in this bone walls were instrumented with bone chisels preoperative diagnostic procedure by taking into in order to remove any soft tissue tags and stimu- account the thickness of the gingiva at the site of late the opening of the marrow cavities, and lastly implantation and the existing gingival architecture irrigated with a saline solution. The socket walls around the natural teeth. Based on the wax-up, a CT and apex were carefully inspected to determine scan of the maxilla (figures 2, 3) and a three dimen- the morphology of the socket and to establish if sional (3D) model were obtained. This allowed for the buccal plate was intact. Upon decision that the construction of a surgical template and precise the site was adequate for the implantation, the sur- planning of the surgical and prosthetic treatment. gical template was inserted and the implant site Simulation of the implantation surgery was per- was sequentially enlarged with pilot and spiral formed and it was possible to individualize the abut- drills according to the standard surgical protocol ment and to fabricate the provisional restoration. for an implant 4.5mm in diameter and 15.0mm in length (Xive S Plus, Dentsply Friadent, Mannheim, Following review of all planning procedures, the Germany). A blasted and acid-etched self-tapping surgery was scheduled. The surgical procedure screw-type implant was placed 1 to 1.5mm away was performed under local anesthesia with mepi- from the buccal bone wall (figure 4). The implant vacaine chlorhydrate with epinephrine 1:100,000. was anchored in the floor of nasal cavity and was Antimicrobial treatment (amoxicillin 875 mg) was given every 12 hours for 10 days, starting 24 hours prior to surgery and was programmed so 62 Vol. 1, No. 8 November 2009

Novaes et al A bioactive glass material grafted over the thin Flap closure and provisional restoration in apical buccal plate. position. found to be stable. Based on the CT scan and days if needed. The patient was placed in on a strict clinical inspection, a thin buccal bone plate in follow-up regime until soft tissue healing was com- the apical third of the implant site was a concern. plete. The final implant impression was made after An apicoectomy-type incision was made at the 3 months and a definitive ceramic abutment (Cer- mucogingival junction and a full-thickness flap was con, Dentsply Friadent, Mannheim, Germany) was raised leaving the coronal aspect of the gingiva connected to the implant and the definitive metal- undisturbed (figure 5). A bioactive glass mate- free ceramic restoration was cemented (figure 8). rial (Biogran, Biomet 3i, Palm Beach Gardens, FL, USA) was grafted over the thin buccal plate (figure A new CT scan was performed 12 months 6) and flap closure was achieved using 5-0 nylon after implant placement in order to verify the sta- sutures. In sequence, the gap between implant and tus of buccal bone plate as well as the osseointe- bone walls was also grafted with the bioactive glass. gration of the implant (figures 9, 10). The implant was stable during all observation periods and no Immediately following implant placement, the complications such as screw loosening, ceramic initial restorative treatment was initiated. The pro- fracture, or pain during chewing were regis- visional restoration which was fabricated based tered. The 12-month post-operative CT scan on the previously performed prototyping was showed complete healing of the periapical lesion then cemented for refinements on contour and and preservation of the cervical buccal plate. occlusal adjustment (figure 7). In sequence, a periapical radiograph was taken using the long- DISCUSSION cone paralleling technique to check the adapta- tion of the prosthetic components and restoration. Providing patients with optimal esthetics remains challenging when teeth require replacement with The patient was instructed to eat a soft diet for implant-supported crowns. However, it can be 4 weeks post surgery. Analgesics were given on a source of great satisfaction for the patient and the day of surgery and postoperatively for the first 3 clinician when the outcome is excellent. Mainte- The Journal of Implant & Advanced Clinical Dentistry 63

Novaes et al The de nitive restoration. Figure 9: Twelve month cross-sectional CT. nance of soft tissue contours is a requisite in gain- evident during the initial phase of wound healing ing an ideal esthetic result. In turn, maintenance than during later periods following tooth removal. of soft tissue contours is dependent on extraction Johnson20 reported that most dimensional altera- techniques that generate less trauma to bone and tions, horizontal as well vertical, occurred during soft tissues followed by providing interim sup- the first three months of healing.20 Carlsson et al port for the overlying soft tissue. Optimal sup- evaluated tissue changes through the analysis of port of the soft tissues during healing following human biopsy specimens of the anterior maxillary tooth extraction in the esthetic region might best extraction sites.21 During an observation period of be provided through immediate implant place- 3 to 210 days, the authors reported that the first ment and insertion of an immediate minimally func- sign of osteoclastic activity was after 7 days and tional fixed provisional and the flapless approach. after about 20 days, additional resorption resulted in a considerable thinning of the buccal bone Araújo et al.17 demonstrated that marked hard plate. After about 40 days, practically all of the tissue alterations occurred during healing follow- original plate was resorbed and partially replaced ing tooth extraction and implant installation in fresh sockets using full thickness flap. The mod- eling in the marginal defect region was accom- panied by marked attenuation of the dimensions of both buccal and lingual bone plate. However in addition to other factors such as position of the implants within the sockets, the results may be due to the full thickness flap that was raised. Loss or reduction of the bony walls due to tooth extraction is not a new observation.18 The healing process following tooth removal results in more pro- nounced resorption on the buccal than the lingual/ palatal aspects of the ridge.19 Further, the process that resulted in tissue reduction seemed to be more 64 Vol. 1, No. 8 November 2009

Novaes et al Figure 10: Negative image of gure 9. tissue attachment at the bone surface will induce an acute inflammatory response which, in turn, by new bone. This new bone, however, was not will mediate resorption of the surface layer of the continuous and lamellar as the original one. More alveolar bone in the exposed area.5,23-25 Wilder- recently, Botticelli et al assessed dimensional man et al, when studying the healing of mucogin- alterations that occurred in the alveolar ridge gival flaps and its effects on the bone, found that during a 4-month period following implant place- within the first week, 5mm of buccal bone height ment in fresh extraction sockets.22 The authors was lost.26 Half of this lost was recovered during concluded that the buccal bone dimension had the healing process, but after 185 days, a loss of undergone horizontal resorption that amounted 2.5mm in height was realized. This loss in height to about 56% while the corresponding reduc- of the buccal bone occurred in the presence of the tion of the lingual/palatal bone plate was 30%. tooth and the periodontal ligament, proving that the loss in buccal bone height is due to the mucog- This loss is greatly due to the full thickness flap ingival flap that compromises the vascularization that is frequently used. It is well documented that of the periosteum to the bone. Similar findings surgical trauma which includes the separation of regarding the healing of mucogingival flaps and the periosteum and the rupture of its connective the sequence of events was shown by Kon et al.27 The buccal plate in the cervical area is very thin and mainly cortical. It has no vascularization or mar- row spaces, so it depends on the vascularization that comes in part from the periodontal ligament and the periosteum. When tooth extraction is per- formed, a good part of vascularization of the buccal plate is lost. Additionally, if a full thickness flap is raised, the remaining vascularization of the buccal plate is removed leading to a resorption process.28 With the flapless approach, the vascularization from the periosteum to the thin buccal plate is pre- served, minimizing the possibility of resorption. Correspondence: Arthur Belém Novaes Jr. Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo, Avenida do Café s/n, 14040-904, Ribeirão Preto, SP, Brasil. [email protected] The Journal of Implant & Advanced Clinical Dentistry 65

Novaes et al Disclosure 12. Lazzara R. Immediate implant placement 24. Staffileno H, Levy S, Gargiulo A. Histologic The authors report no conflicts of interest with into extraction sites: surgical and restorative study of cellular mobilization and repair anything mentioned in this paper. advantages. Int J Periodontics Restorative following a periosteal retention operation via Dent1989; 9: 332-43. split thickness mucogingival flap surgery. J References Periodontol 1966; 37: 117–131. 1. Spear F. Maintenance of the interdental 13. Parel S, Triplett R. Immediate fixture placement: a treatment planning alternative. Int J Oral 25. Wood DL, Hoag PM, Donnenfeld OW, papilla following anterior tooth removal. Pract Maxillofac Implants 1990; 5: 337-345. Rosenberg DL. Alveolar crest reduction Periodontics Aesthet Dent 1999; 11:2 1-28. following full and partial thickness flaps. J 14. Huys L. Replacement therapy and the Periodontology 1972; 43: 141–144. 2. Carlsson G, Bergman B, Hedegard B. Changes immediate post-extraction dental implant. in contour of the maxillary alveolar process under Implant Dent 2001; 10: 93-102. 26. Wilderman MN, Wentz FM, Orban BJ. immediate dentures. A longitudinal clinical and Histogenesis of repair after mucogingival x-ray cephalometric study covering 5 years. Acta 15. Chaushu G, Chaushu S, Tzohar A, Dayan D. surgery. J Periodontol 1960; 31: 283-299. Odontol Scand 1967; 25: 45-75. Immediate loading of single-tooth implants: immediate versus non-immediate implantation. 27. Kon S, Novaes AB, Ruben MP, Goldman HM. 3. Becker W, Ochsenbein C, Tibbetts L, Becker A clinical report. Int J Oral Maxillofac Implants Visualization of the microvascularization of the B. Alveolar bone anatomic profiles as measured 2001; 16: 267-272. healing periodontal wound. IV. Mucogingival from dry skulls. Clinical ramifications. J Clin surgery: full thickness flap. J Periodontol 1969; Periodontol 1997; 24: 727-731. 16. Andersen E, Haanaes H, Knutsen B. 40: 441-456. Immediate loading of single-tooth ITI implants 4. Salama H, Salama M, Garber D, Adar P. The in the anterior maxilla: a prospective 5-year 28. Araújo MG, Lindhe J. Dimensional ridge interproximal height of bone: a guidepost to pilot study. Clin Oral Implants Res 2002; 13: alterations following tooth extraction. predictable aesthetic strategies and soft tissue 281-287. An experimental study in the dog. J Clin contours in anterior tooth replacement. Pract Periodontol 2005; 32: 212-218. Periodontics Aesthet Dent 1998; 10: 1131- 17. Araújo M, Sukekava F, Wennström J, Lindhe J. 1141. Tissue modeling following implant placement in fresh extraction sockets. Clin Oral Implants Res 5. Brägger U, Pasquali L, Kornman K. Remodeling 2006; 17: 615-624. of interdental alveolar bone after periodontal flap procedures assessed by means of computer- 18. Schropp L, Wenzel A, Kostopoulos L, Karring T. assisted densitometric image analysis (CADIA). J Bone healing and soft tissue contour changes Clin Periodontol 1988; 15: 558-564. following single-tooth extraction: a clinical and radiographic 12-month prospective study. Int 6. Wllderman M. Exposure of bone in periodontal J Periodontics Restorative Dent 2003; 23: surgery. Dent Clin North Am 1964; 3: 23-26. 313-323. 7. Buser D, Brägger U, Lang N, Nyman S. 19. Pietrokovski J, Massler M. Alveolar ridge Regeneration and enlargement of jaw bone using resorption following tooth extraction. J Prosthet guided tissue regeneration. Clin Oral Implants Dent 1967; 17: 21–27. Res 1990; 1: 22-32. 20. Johnson K. A study of the dimensional changes 8. Dahlin C, Andersson L, Linde A. Bone occurring in the maxilla following tooth augmentation at fenestrated implants by extraction. Aust Dent J 1969; 14: 241-244. an osteopromotive membrane technique. A controlled clinical study. Clin Oral Implants Res 21. Carlsson G, Thilander H, Hedegard B. 1991; 2: 159-165. Histologic changes in the upper alveolar process after extractions with or without 9. Jovanovic S, Spiekermann H, Richter E. Bone insertion of an immediate full denture. Acta regeneration around titanium dental implants in Odontol Scand. 1967; 25: 21-43. dehisced defect sites: a clinical study. Int J Oral Maxillofac Implants 1992; 7: 233-245. 22. Botticelli D, Berglundh T, Lindhe J. Hard- tissue alterations following immediate 10. Rogers W, Applebaum E. Changes in the implant placement in extraction sites. J Clin mandible following closure of the bite with Periodontol. 2004; 31: 820-828. particular reference to edentulous patients. J Am Dent Assoc 1941; 28: 1573. 23. Wilderman M. Repair after a periosteal retention procedure. J Periodontol 1963; 34: 11. Tylman S, Tylman S. Theory and Practice of 487–503. Crown and Bridge Prosthodontics 1960; 4th edition, 69–71. St. Louis: The C.V. Mosby Company. 66 Vol. 1, No. 7 October 2009

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Subperiosteal Dental Implants: Giulio et al A 25 Year Retrospective Survival Evaluation Antonio T. Di Giulio1 1 2 Abstract Background: Making long term retentive den- Results: 66 patients received a chrome- tures for patients with inadequate bone for cobalt total subperiosteal implant between endosseous dental implants is a challenge. In 1984 and 1995. 54 patients received a tita- such situations, utilization of subperiosteal den- nium total subperiosteal implant between tal implants is a viable yet often overlooked 1996 and 2008. Statistical analysis of Kaplan- option. The aim of this study was to determine Meier demonstrated a survival rate of 95.5% the long term survival rates of subperiosteal at 7 years and 89.1% at 20 years for chrome- dental implants placed between 1985-2008. cobalt implants. Titanium subperiosteal dental implants had a survival rate of 81.1% at 7 years. Material and methods: All candidates for subperiosteal dental implants underwent com- Conclusions: This study demonstrates that puted tomography (CT) scans to reproduce subperiosteal dental implants offer a viable alter- the bone crest in maximum detail. A ste- native to endosseous dental implants when reolithographic model for both maxilla and inadequate bone is present. Presurgical evalu- mandible was constructed, upon which a sub- ation with computerized tomography and utiliza- periosteal prosthesis was then constructed. tion of stereolithic models allows for reduced surgical time and properly fitting structures. KEY WORDS: Subperiosteal dental implants, chrome-cobalt, titanium, maxilla, mandible, stereolithography 1. San Babila Day Hospital, via Stoppani 36, Milano, Italy 2. Farmaco-Biologico Department, Università degli Studi di Bari, Italy The Journal of Implant & Advanced Clinical Dentistry 69

Giulio et al INTRODUCTION Figure 1: Maxillary stereolithographic model. In 1965, Brånemark1 placed the first titanium Figure 2: Mandibular stereolithographic model. dental implant into a human maxilla ushering in a new era in the field of dentistry. Decades of ined 120 consecutive patients. A total of 65 data provide overwhelming evidence that implan- female patients (mean age of 51.5 ± 11.0 years) tology is a safe therapeutic intervention and pro- and 55 males (mean age of 49.3 ± 12.0 years) vides recipients with function, aesthetics, and were evaluated. All patients treated in this study comfort following a minimally invasive surgical were completely edentulous and typically pre- approach. Furthermore, computer-assisted navi- gation systems, which improve intra-operative safety by preventing damage to nerves and other critical structures, have recently been successfully applied to implant dentistry. At a technical level, this has led implantology to achieve maximum pre- cision. However, although surgical dental implant placement is safe and rigorously programmed, it is sometimes not without complications deriving from the many variables involved in the procedure. Though there are many ways of making implants feasible, inadequate osseous structures sometime render this option inaccessible. In such situa- tions, utilization of subperiosteal dental implants is a viable yet often overlooked option. The first subperiosteal implant in Europe was carried out by Dahl2 back in 1940 followed by Goldberg and Gershkoff3 later utilizing this treatment modality in the USA. Linkow4 further advanced use of the subperiosteal implant with the design referred to as the “tripodal mandibular subperiosteal implant.” This article focuses on over 25 years of the authors’ clinical experience with subpe- riosteal dental implants including the sur- gical procedure, post-operative follow up, and statistical analysis of long term survival. MATERIALS AND METHODS A retrospective survival study of subperiosteal dental implants placed from 1984 to 2008 exam- 70 Vol. 1, No. 8 November 2009

Giulio et al Figure 3: Example of maxillary subperiosteal implant t. Figure 4: Suturing following maxillary subperiosteal implant delivery. sented with severely resorbed maxillas and/or mandibles. Smokers and those suffering from tal implant, constructed of either chrome-cobalt chronic systemic conditions such as diabetes, or titanium, has a palatal bar connected to two cardiovascular disease, severe osteoporosis, or vestibular bars simulating roots of the molars (fig- those undergoing chemo/radiation therapies were ure 1). The framework of the mandibular subpe- not included in this study. Candidates for subpe- riosteal dental implant (figure 2) embraces the riosteal implant therapy received panoramic radio- alveolar crest, reminiscent of the tripodal mandib- graphs and computed tomography (CT) scans ular subperiosteal implant proposed by Linkow.4 with 64 multislices (General Electric Co, USA) to reproduce osseous structures in maximum detail. All patients were treated under local anesthesia Such pretreatment analysis allowed us to become with occasional use of sedation. An incision was familiar with the patient’s three-dimensional (3D) made on the alveolar crest and mucoperiosteal bony architecture and critical anatomical struc- flaps were elevated to facilitate fixture delivery. It tures so as to plan the subperiosteal implant. should be noted that before this procedure was introduced (2003), the protocol described by This analysis allowed for fabrication of maxil- Linkow4 and Moore5 had been followed. With the lary and mandibular stereolithographic models newer procedure, the fit of the implant was evalu- used in constructing custom fabricated subpe- ated by pulling it to make sure of perfect contact riosteal dental implants. The exacting detail of with the bone. Before suturing of the gingiva, the the models allowed for fixtures that intimately implant was covered with hydroxyapatite (n=34 adapted to the patients’ osseous anatomy before patients) or demineralized bone allograft (n=15 any surgical procedure was ever undertaken. patients), whereas in another 5 subjects no graft The structure of the maxillary subperiosteal den- was used (Figures 3 and 4). Postsurgical instruc- tions were given to the patient and follow-up CT’s The Journal of Implant & Advanced Clinical Dentistry 71

Giulio et al and panoramic radiographs were performed in Figure 5: New bone covering subperiosteal implant from all cases. A 4-month healing period was allowed gure 3. prior to placing prosthetic restorations for full function. The evolution of the treatment was eval- Five implants failed in males (3 maxillary, 2 man- uated by pulling the implant in all possible direc- dibular) and 2 failed in females (1 maxillary, tions and additional radiographs were taken to 1 mandibular). Allergy to chrome-cobalt was identify bone apposition over the abutment. Fig- determined to be the cause of 5 implant failures ure 5 shows healed bone covering portions of while other causes included: a) 1 case of meno- the subperiosteal dental implant from figure 3. pausal osteoporosis; b) 1 case of excessive long term osseous resorption in an elderly subject Annual check-ups were required to verify the (73 years of age). In the latter two cases, the success of the implant. The parameters assess- implants were removed after 13 and 19 years ing implant success were based on subjective and respectively. Statistical analysis was performed objective clinical criteria such as: 1) absence of on the chrome-cobalt study cohort minus deaths clinically-detectable implant mobility; 2) absence and patients failing to respond to recall. Survival of pain; 3) absence of inflammation; 4) comfort of rate at 7 years of observation was 95.5% while patient; 5) bleeding on probing; 6) pocket-prob- survival rate at 20 years was 78.1% (figure 6). ing depth; 7) absence of foreign body sensation. Fifty four patients received titanium total sub- Statistical analysis of survival rates at 7 and periosteal implants between September 1996 20 years were performed applying the method and March 2008. Of those, 57.4% (n=31) were of Kaplan-Meier.6 Graphpad PrismTM version female and 42.6% (n=23) were male patients. 3.0 (Graph Pad Software, Inc, http://www.graph- Some patients in this study cohort received a pad.com) was used to calculate survival fractions using the product limit and report the uncertainty of the fractional survival as standard error calcu- lated by the method of Greenwood. Furthermore, comparison among different survival curves was automatically performed by means of logrank test. Success rates were calculated as a percentage. RESULTS Sixty six patients received chrome-cobalt total subperiosteal implants between April 1984 and February 1995. Of those, 51.5% (n=34) were female and 48.5% (n=32) were male patients. 43 of the 66 implants were placed in the max- illa and 23 in the mandible. The total number of failed chrome-cobalt subperiosteal implants during the total observation period was seven. 72 Vol. 1, No. 8 November 2009

Giulio et al Figure 6: Kaplan–Meier estimate of survival rates of Figure 7: Kaplan–Meier estimate of survival rates of chrome-cobalt implants as a function of time since chrome-cobalt and titanium implants as a function of time installation. since installation. treatment modification as select cases were of 2 = 2.43 and a p-value of P = 0.12, indicating grafted with hydroxyapatite or demineralized bone that the two curves are not significantly different. allograft. As this was a newer procedure, only seven year survival rate was determined. The total DISCUSSION number of failed titanium subperiosteal implants during this observation period was four (2 male, Multiple studies have shown that the various 2 female). The causes of failure were determined endosseous dental implants available today suc- to be: a) 3 cases of severe osteoporosis; b) 1 cessfully osseointegrate and have good long term implant fracture after one year of function. Sta- prognoses. In most of these studies, patients tistical analysis was performed on the titanium typically have adequate bone for implant fixture study cohort minus deaths and patients failing delivery or osseous structures conducive to rea- to respond to recall. Survival rate at 7 years of sonable grafting procedures. For patients with observation was 87.1%. As a side note, it should inadequate mandibular and/or maxillary bone, be mentioned that use of demineralized bone treatment with endosseous dental implants is not allograft did not occur until the period of 2002- always feasible. In such situations, treatment with 2008. Although follow up on these cases is short subperiosteal dental implants may be the patient’s compared with the previous subperiosteal implant only option for fixation of dental prostheses.7,8 techniques, it is worth noting that 100% of these cases have survived and are still in function. This study reported on survival rates of 120 subperiosteal dental implants placed over 24 A comparison of the survival curves of chrome- years (1985-2008). The survival rates seen in cobalt and titanium subperiosteal dental implants this study are comparable to results published is reported in figure 7. The analysis gives a value by other authors who reported a survival rates of 87%, 98%, 79%, 78%, and 98.7% over approxi- The Journal of Implant & Advanced Clinical Dentistry 73

Giulio et al mately 10 years, respectively.9-12 Although a viable alternative treatment option. Over a 24 year retrospective evaluation, the survival rates these survival rates are less than those typically of subperiosteal dental implants seen in this and other studies prove this treatment modal- reported with endosseous dental implants, one ity to be a feasible treatment option in select patient populations. The most important aspect must remember that most cases treated with sub- for long term success of subperiosteal dental implants is precise manufacturing of the implant periosteal dental implants have osseous struc- to fit the patient’s osseous profile. Additionally, proper prosthetic restoration and periodic follow tures of an often compromised nature. In many up visits are required. All of the patients seen in this study profess complete satisfaction with of these cases, treatment with endosseous dental their implants in terms of improvements to their social life and stomatognathic functionality. This implants was neither a feasible nor a safe option. is of considerable importance owing to the rela- tively young age of our patients. Indeed, to para- It is worth noting that in some patients who phrase Brånemark’s famous remark, “nobody should have to live a nightly bedtime drama showed chrome-cobalt allergy or severe osteo- with his/her overdentures in a glass of water.” porosis, their implants lasted a mean of 5.0 ± 2.3 Correspondence: Dr. Enrico Gallucci years after surgery. Complications due to chrome- Dipartimento Farmaco-Biologico Università degli Studi di Bari cobalt allergy were overcome by the use of tita- via E. Orabona 4, 70126 Bari, Italy Tel/Fax: +39 0805442796 nium, which has excellent biocompatibility and Email: [email protected] high corrosion resistance.13-16 Additionally, the recent addition of demineralized bone allograft to the subperiosteal implant procedure has improved survival rates at the 7 year benchmark. Further evaluation at the 20 year benchmark will pro- vide additional data for long term survival of con- temporary use of subperiosteal dental implants. The successful delivery of subperiosteal den- tal implants is aided by three-dimensional com- puted tomography reconstructions enabling the precise reconstruction of the patient’s osseous profile upon which the subperiosteal implant is to be placed. Particular mention should be made of the stereolithographic technique, which enables a model to be created from a CT data set. This template of the mandible and/ or maxilla provides precise guidance for sub- periosteal implant design and delivery in vivo. CONCLUSION For patients with severe inadequacies of man- dibular and/or maxillary bone, treatment with endosseous dental implants is not always fea- sible and the subperiosteal dental implant offers 74 Vol. 1, No. 8 November 2009

Giulio et al Disclosure The authors report no conflicts of interest with anything mentioned in this article. Acknowledgements The authors would like to thank their colleague Anthony Green for proofreading and providing linguistic advice. The following collaborators: Engineer F. Davolio, Radiologist A. Zerbi, Technician E. Puntieri are gratefully acknowledged for their collaboration. References 1. Brånemark P. Available at: http://en.wikipedia.org/wiki/Dental_ implant#cite_ref-2 2. Dahl G. Dental implant and superplants. Rassegna Trimestrale Odontoiatria 1956; 4: 25-36. 3. Goldberg N, Gershkoff A. Implant lower denture. Dent Dig 1949; 55: 490- 494. 4. Linkow L, Wagner J, Chanavaz M. Tripodal mandibular subperiosteal implant: basic sciences, operational procedure, and clinical data. J Oral Implantol 1998; 24:16-36. 5. Moore JD, Hansen PA. A descriptive 18-year retrospective review of subperiosteal implants for patients with severely atrophied edentulous mandible. J Prosthet Dent 2004;92:145-150. 6. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Amer Stat Assoc 1958; 53: 457-48. 7. Kurtzman G, Schwartz K. The subperiosteal implant as a valuable long-term treatment modality in the severely atrophied mandible: a patient’s 40-years case history. J Oral Impantol 1995; 21: 35-39. 8. Kusek E. The use of laser technology (ER;CR:YSGG) and stereolithography to aid in the placement of a subperiosteal implant: A case study. J Oral Implantol 2009; 35: 5-11. 9. James R. Subperiosteal implant design. NY J Dent 1983; 53: 407-14. 10. Golec T, Krauser J. Long-term retrospective studies on hydroxyapatite coated endosteal and subperiosteal implants. Dent Clin North Am 1992; 36: 39-65. 11. Yanase R, Bodine R,Tom J, White S. The mandibular subperiosteal implant denture: a prospective survival study. J Prosthet Dent 1994; 71: 369-74. 12. Bodine R, Yanase R, Bodine A. Forty years of experience with subperiosteal implant dentures in 41 edentulous patients. J Prosthet Dent 1996; 75: 33-44. 13. Albrektsson T, Hansson H, Ivarsson B. Interface analysis of titanium and zirconium bone implants. Biomaterials 1985; 6: 97-101. 14. Steinemann S, Eulenberg J, Maeusli P, Schroeder A. Biological and Biochemical Performance of Biomaterials, 1st edition, Elsevier, Amsterdam 1986; 409-414 . 15. Rae T. The biological response to titanium and titanium-aluminium- vanadium alloy particles I. Tissue culture studies. Biomaterials 1986; 7: 30-36. 16. Lindigkeit J. Titanium and titanium alloys: Fundamentals and Applications, Wiley-VCH Verlag GmbH & Co. KGaA 2005; 453-466. The Journal of Implant & Advanced Clinical Dentistry 75

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Dental 3D Imaging Centers - Usage and FindingsW:inter et al Part III – Bi d Canals and Other Deviations of the Inferior Alveolar Nerve Alan A. Winter, DDS1 23 45 6 Abstract Background: This is part 3 of a 5 part study evalu- did not demonstrate evidence of a bifid canal. In ating data obtained from dental referral usage of contrast, 110 patients (37.16%) had one or more radiological labs for three dimensional (3D) ana- bifid canals. Of the 110 patients demonstrating bifid tomical scans. The purpose of this current study canals, 56 (50.9%) had one bifid canal, 37 (33.6%) was to gather data on bifid mandibular canals and had two canals, and 17 (15.45%) had three or more other deviations of the inferior alveolar nerve (IAN). canals. Slightly more than half (55.45%) of bifid canals were unilateral. Two thirds (67%) of the uni- Methods: Data from 500 consecutive patients lateral bifid canals were on the right side of the man- sent to i-dontics dental radiological centers from dible; one third (33%) of the unilateral bifid canals 9 centers locations in 3 states were evaluated. were on the left side of the mandible. 9 bifid canals Of these patients, the current study evaluated (8.18%) were located at the mental foramen, 94 296 mandibles for the following: the incidence (85.45%) were posterior to the mental foramen, and of bifid branches of the inferior alveolar canal, the 7 (6.36%) continued anterior to the mental foramen. number of branches present when the IAN was observed to split, laterality of the bifid canals, and Conclusions: The incidence of bifid mandibular the location of the bifid canal in relation to the canals (37%) from the current study was greater mental foramen (anterior, equal to, or posterior). than that reported in other studies. Presurgical identification of bifid canals reduces risk of dam- Results: 296 mandibular scans were included in age to vital structures and may explain difficulty the study. Of these scans, 186 patients (62.84%) in obtaining local anesthesia in certain situations. KEY WORDS: Cone beam computed tomography, inferior alveolar nerve, bifid canals mandible, dental implants 1. Assistant Clinical Professor, Department of Periodontics and Implant Dentistry, New York University College of Dentistry 2. Private practice, New York, USA 3. Private practice, New York, USA 4. Private practice, New York, USA 5. Private practice, New York, USA 6. Director Maxillofacial Dental Radiology and Associate Professor of Clinical Dentistry, Columbia School of Dental Medicine The Journal of Implant & Advanced Clinical Dentistry 77

Winter et al INTRODUCTION Figure 1: Prevalence of bi d canals in 296 patients. The recent advent of cone beam computed Figure 2: Of the mandibles demonstrating bi d canals, tomography (CBCT) technology has vastly 50.9% had one branch, 33.6% had branches, and 15.45% increased the diagnostic options for dental treat- had three or more branches. ment. While this technology is continually improv- ing in terms of quality, equipment size, and cost, anesthetic injection technique, prosthetic design, most dental offices do not own CBCT scanners and surgical procedures can be modified to pre- at this time. Accordingly, many practices cur- vent pain and discomfort during treatment pro- rently refer patients to freestanding dental radio- cedures10 and ultimately improve final outcomes. logical labs for three dimensional (3D) anatomical scans. The purpose of this series of studies was MATERIALS AND METHODS to determine how and for what reason den- tists currently utilize dental 3D imaging centers. CBCT scans of the dental arches from 500 consecutive patients taken in 9 centers located Part one of this study series evaluated demo- in 3 states were uploaded to the main pro- graphic data and the reasons why patients were referred for 3D evaluation. Part two of this study series evaluated anatomical features of the lin- gual artery in relation to dental implant treat- ment. The purpose of this current study was to gather data on bifid mandibular canals and other deviations of the inferior alveolar nerve (IAN). A bifid mandibular canal is a relatively uncom- mon anatomical variation typically seen in less than 1% of the population. The incidence of bifid canals has been evaluated with both con- ventional panoramic and computed tomography (CT) images. Findings indicate that the canals may split in different positions along the length of the IAN and one branch may be smaller than the other.1,2 Langlais et al3 reported a 0.95% preva- lence of bifid mandibular canals while Sanchis4 reported an incidence of 0.4% in an evaluation of 2,012 mandibles. Multiple studies agree that the bifid anatomical variations need to be identi- fied when surgical procedures such as removal of impacted third molars, insertion of dental implants, and osteotomies, are to be performed.5-9 Once bifid canals are identified, the local 78 Vol. 1, No. 8 November 2009

Winter et al Figure 3: 55% (61/110) of bi d canals were unilateral tinuous with the main inferior alveolar canal while nearly 46% (49/110) were identi ed bilaterally. The in each slice. For consistency, all studies majority of unilateral canals were located on the right side were examined by a single examiner (KY). of the mandible (41/61). RESULTS cessing center of a single dental radiologi- cal practice (i-dontics, llc., New York, N.Y.) Number which is limited to taking and processing 3D 296 mandibular scans were included in the CT images for the dental community. Scans study. Of these scans, 186 patients (62.84%) were taken on either i-CAT scanners (8 cen- did not demonstrate evidence of a bifid canal. ters) or on a (1) NewTom 3G scanner. All stud- In contrast, 110 patients (37.16%) had one ies were converted to SimPlant™ (Materialise, or more bifid canals. Of the 110 patients Glen Burnie, MD). When not specified, the demonstrating bifid canals, 56 (50.9%) had data was converted to SimPlant™ version 10. one bifid canal, 37 (33.6%) had two canals, and 17 (15.45%) had three or more canals. In the current study, 296 of the 500 scans were of the mandible. These scans were eval- Laterality uated for the following: the incidence of bifid Slightly more than half (55.45%) of bifid canals branches of the inferior alveolar canal, the num- were unilateral. Two thirds (67%) of the unilat- ber of branches present when the IAN was eral bifid canals were on the right side of the observed to split, laterality of the bifid canals, and mandible; one third (33%) of the unilateral bifid the location of the bifid canal in relation to the canals were on the left side of the mandible. mental foramen (anterior, equal to, or posterior). Location of the Bifid Canal All CBCT studies were made into 1.0 9 bifid canals (8.18%) were located at the mm slides and viewed both in the coro- mental foramen, 94 (85.45%) were poste- nal and transaxial planes. To be counted as rior to the mental foramen, and 7 (6.36%) a bifid canal, each offshoot had to be con- continued anterior to the mental foramen. DISCUSSION The incidence of bifid canals has been reported at less than one percent3,4 and the split of the mandibular nerve may be of unequal sizes.1,2 Regardless of the frequency of identify- ing bifid canals, various authors have identi- fied the surgical risks and complications that may be experienced when they are encoun- tered, including an inability to obtain pro- found anesthesia using a local anesthetic.5-9 The Journal of Implant & Advanced Clinical Dentistry 79

Winter et al Figure 4: The majority of the bi d canals (85%) ended posterior to the mental foramen, while 8 percent terminated at the mental foramen, and 6% extended anterior the mental foramen. In order to achieve standardization and con- were then verified by a second author (AW). sistency, the authors agreed as to what consti- The significance of the findings in this study tutes a bifid canal as identified on the 3D image: any branch that appeared as a continuous radio- matters relative to the size and location of the lucent canal extending from the inferior alveolar bifid canals, and what clinical procedure is nerve. All slices were 1mm in thickness and all anticipated. Concerning operative dentistry, bifid canals were viewed and appeared to ema- it has been postulated that bifid nerves may nate from the IAN in three planes: axial, coronal, explain why anesthesia is not as profound as it and sagittal. Once the parameters were defined, should be when employing a local anesthetic. one researcher (YK) examined and identified all When encountered, infiltration of the local anes- of the bifid canals noted in this study, which thetic to anesthetize these extra branches of the IAN may help achieve greater local anes- 80 Vol. 1, No. 8 November 2009

Winter et al Figure 5: Arrow indicates a small bi d canal that starts and ends distal to tooth #31. A larger canal can be seen anterior to tooth #18. Figure 6: The left bi d canal is highlighted in red, illustrating 3 bi d canals. thesia. When planning implant surgery, it is Note the arrow in Figure 5 that highlights a helpful to identify if any bifid canals exist in the bifid canal. Careful inspection will note addi- surgical site. Encountering these extra canals tional canals emanating from the right IAN. may not only contribute to unwanted local par- esthesias, but may also explain unusual bleed- Mention must be made of the value of 3D ing that emanates from the alveolar bone.10-11 images identifying normal and abnormal struc- tures when compared to 2D images. Figure Figures 5 and 6 illustrate an example of 7 is a panoramic image (formatted in a 15 mm multiple canals as they were identified in this trough) taken on a patient that was referred study. While the widest branch, which is ante- to the CT lab after an implant was inserted rior to tooth #18, is evident on the panoramic that resulted in paresthesia in the patient. slice, smaller canals are highlighted in Figure 6. Figure 8 highlights a bifid branch of the IAN The Journal of Implant & Advanced Clinical Dentistry 81

Winter et al Figure 7: Patient presented after an implanted was inserted in the #30 site resulting in paresthesia. Figure 8: A bi d nerve rises from the IAN and was traumatized by the implant insertion. that was traumatized by an implant. This aber- implant insertion would have identified the bifid rant branch was not evident in the panoramic (aberrant) branch and altered the surgical site. view due to the dense cortical bone. Traditional 2D imaging, both panoramic and periapical film, CONCLUSION is limited in revealing key anatomic structures that are obscured by thick buccal and/or lingual The incidence of bifid mandibular canals (37%) bone. In this example, using 3D imaging prior to from the current study was greater than that 82 Vol. 1, No. 8 November 2009

Winter et al reported in other studies. Presurgical identifi- The Journal of Implant & Advanced Clinical Dentistry cation of bifid canals reduces risk of damage to vital structures and may explain difficulty in obtaining local anesthesia in certain situations. Correspondence: Dr. Alan Winter [email protected] Disclosure: For complete details Support for this study was generously given by NobelBiocare, Mahwah, NJ regarding publication in and Imaging Sciences Inc., Hatfield, PA. JIACD, please refer References: to our author guidelines at 1. Mardini S, Gohel A. Exploring the Mandibular Canal in 3 Dimensions. the following link: An Overview of Frequently Encountered Variations in Canal Anatomy. http://www.jiacd.com/ AADMRT Newsletter, Fall 2008. authorinfo/ 2. Jacobs R, Mraiwa N, vanSteenberghe D, Gijbels F, Quirynen M. author-guidelines.pdf Appearance, location, course, and morphology of the mandibular incisive canal: an assessment on spiral CT scan. Dentomaxillofacial Radiology or email us at: 2002; 31:322-327. [email protected] 3. Langlais RP, Broadus R, Glass B. Bifid mandibular canals in panoramic radiographs. J Am Dent Assoc 1985; 110:923-926. 4. Sanchis JM, Penarrocha M, Soler F. Bifid mandibular canal. J Oral Maxillofac Surg 2003; 61:422–424. 5. Rouas P, Nancy J, Bar D. Identification of double mandibular canals: literature review and three case reports with CT scans and cone beam CT. Dentomaxillofacial Radiology 2007; 36:34-38. 6. Naitoh M, Hiraiwa Y, Aimiya H, Gotoh M, Ariji Y, Izumi M, Kurita K, Ariji E. Bifid Mandibular Canal in Japanese. Clinical Science and Techniques Implant Dentistry 2007; 16:24-32. 7. Claeys V, Wackens G. Bifid mandibular canal: Literature review and case report. Dentomaxillofacial Radiology 2005; 34:55-58. 8. Auluck A, Ahsan A, Pai KM, Shetty C. Anatomical variations in developing mandibular nerve canal: A report of three cases. Neuroanatomy 2005; 4:28–30. 9. Dario LJ. Implant placement above a bifurcated mandibular canal: A case report. Implant Dent 2002; 11:258-261. 10. Auluck A, Ahsan A, Pai KM, Mupparapu M. Multiple mandibular nerve canals: Radiographic observations and clinical relevance. Report of 6 cases. Quintessence International 2007; 38:781-787. 11. Winter AA. Bleeding from a Nutrient Canal: A Case Report. NY State Dent J 1980; 46:646. The Journal of Implant & Advanced Clinical Dentistry 83