Special reprint from THE INTERNATIONAL JOURNAL OF PERIODONTICS RESTORATIVE DENTISTRY Vol. 16 Copyright© 1996 Quintessence Publ Co, Inc 96 47 Histologic Evaluation of Sinus Elevation Procedure: A Clinical Report Stephen S. Wallace, DOS' Stuart J.Froum,DDS'* Dennis P. Tarnow, DDS*** A histologic assay of the grafting material associated with the sinus elevation procedure would provide insight into the quality and quantity of vital bone at the implant-bone interface. This case report documented for the first time the sequential healing process of a sinus graft in the same patient at 4,8, 12, and 20 months. Histology of trephineobtained core samples showed that in a sinus grafted with a mixture ofxenograft (80%) and autograft (20%). 12 to 20 months was required for remodeling to vital bone. The study also demonstrated that a significant amount of vital, mature bone was generated by this procedure. Quantification of the resulting bone and comparison with other grafting techniques should be the next phase of continuing research efforts. (Int J Periodont Rest Dent 1996; 16:47-51.) •Assistant Clinical Professor, Department of Implant Dentistry, New York University College of Dentistry, New York, New York. "Clinical Professor, Department of Prosthodontics (Implants) and Department of Surgical Services (Pehodontics), New York University College of Dentistry, New York, New York. 'Chairman and Associate Professor, Department of Implant Dentistry, New York University College of Dentistry, New York, New York. Reprint requests: Dr Stephen S.Wallace, Central Connecticut Dental Implant Center. 140 Grandview Avenue, Suite 102, Waterbury. CT 06706. The sinus elevation and subantral augmentation procedure first introduced by Tatum1 and later modified by Wood and Moore2 has seen a marked increase in clinical usage. In fact, it has become one of the most common methods for increasing vertical bone height for implant placement in the posterior atrophic maxilla. This growth has been encouraged by high success rates reported in the literature3 and by anecdotal information supplied by leading clinicians. In almost all cases, the reported success was related to apparent rigid fixation (stability) of the implants placed in the augmented sinus. Only recently4 has there been a histologic comparison (dog model) of the results achieved with different grafting materials. While the success is impressive, there are many variables included in this type of reporting which can make it difficult for clinicians to duplicate these results, These variables include but are not limited to the type Volume 16, Number 1. 1996 of bone grafting material utilized, an immediate or delayed placement procedure, the type of implant, the surgical and prosthetic protocols, and the effects of postsurgical and prosthetic loading.' Successful osseointegration is defined by events that occur at the implant-bone interface. Consequently, it is reasonable to assume that the success of the sinus elevation procedure is best defined and understood by the histologic status of the bone at that interface. Using the histologic definition, a successful sinus elevation procedure is one thai provides the maximum quantity and quality of vital bone to take part in the process of osseointegration. Use of the histologic definition precludes many of the variables associated with the sinus lift procedure, and may allow informative examination of the key variabies that lead to the formation of vital bone in the sinus cavity The current report describes the grafting procedure utilized and temporal histologic findings documenting the healing response over a 20-month time period. Case report A 65-year-old man in good health presented with an afrophic maxilla with all posterior teeth missing. In preparation for implanis, a bilateral sinus elevation procedure was performed using a combination of xenogenous and autogenous grafting materials. After allowing 4 months for graft healing, seven one-stage implants were placed in the sinus. At time of implant placement (4 months) and at 8, 12, and 20 months, horizontal bone cores were harvested with a trephine. All the cores were decalcified, sectioned, and stained with hematoxylin- eosm for histologic evaluation. Grafting material Many consider autologous marrow or corticocancellous grafts obtained from the hip to be the "gold standard" of grafting material for the sinus elevation procedure.6 The required hospitalization and increased morbidity of the extraoral procedure makes a completely intraoral procedure that achieves similar results advantageous. Moy et al7 have reported almost 60% bone in the sinus with the utilization of an autogenous graft harvested from the chin. The International Journal of Periodontics & Restorative Dentistry 49 In a paper on the mechanism of the anorganic bovine matrix (xenograft), Cheung and Tofe8 showed that the xenograft has the qualities of the autograft matrix, and consequently may be suitable as a graft material in sinus elevation procedures. In an effort to minimize the requirement for infraoral sourcing, autogenous bone harvested from tuberosities was combined with commercially available xenograft material. The following formulation (by volume) was prepared for grafting: 40% 250 to 420 mm of anorganic bovine matr x (OsteoGraf/N-300, CeraMed), 40% 420 to 1000 mm of anorganic bovine matrix (Osteo- Graf/N-700), and 20% autogenous bone harvested from the tuberosities. The formulation of the autogenous bone and marrow with the anorganic bovine matrix9 provided the basis for the findings seen in this study. Histologic findings Focusing on histology allowed an assessment of the osseous changes that occurred over time during the healing phase following the use of a combination of xenograft and autograft for a sinus elevation procedure. This study in the same patient at different stages of the 20-month healing period allowed, for the first time, a temporal evaluation of the bone turnover process. Figures la to 1 d depict the sequential histologic events involved in the turnover/replacement (remodeling) of the anorganic bovine (xenograft) bone matrix and vital autogenous bone in the maxillary sinus. Figure 1 a illustrates that the nonvital bone present at 4 months is the remnant of the original autograft, with only a very small percentage of vital bone formed at this time. The 8-month (Fig 1 b) and 12-month (Fig lc) intervals show increasing vascularity and vital bone content, with a concurrent decrease in residual autograft and xenograft material. It is interesting to note the increased presence of osteoclastic activity especially in the 12-month section. The 20- month section (Fig Id) shows an increase in volume and maturation of vital bone, a complete lack of xenograft, and the presence of a fatty, mature, and relatively avascular marrow. Volume 16, Number 1, 1996 50 Fig la Histologic section at A months. Bone (solid arrows) and xenograft (outlined arrows) are evident. Note that most of the bone is nonvital. as evidenced by empty lacunae (hematoxylin-eosin stain: original magnification x 33). Fig 1b Histologic section at 8 months Bone (solid arrows) has increased, xenograft (outline arrows) has decreased. Note that the cells in lacunae indicates that alt of the bone is vital (hematoxylin-eosin stain; original magnification x 33). Fig 1c Histologic section at 12 months. Bone volume has increased, xenograft volume has decreased. Note that the marrow (solid arrows) is vascular (hematoxylin-eosin stain; original magnification x 33). Fig Id Histologic section at 20 months. Bone volume and density have increased, and the xenograft was completely resorbed. Note that the marrow (solid anow) is fatty and mature (hematoxylin-eosin stain: original magnification x 33). The International Journal of Periodorrics & Restorative Dentistry Discussion Conclusion References The temporal histology presented indicates that, in this case, remodeling of the xenograft (OsteoGraf/N) appears to have occurred during the 12- to 20-month interval. Visually, the percentage of bone seen in the later slides is significant It is also evident that by 12 months all remaining nonvital autograft has been replaced or resorbed. The time required for resorption of the xenograft (12 to 20 months) seems to favor the delayed approach to implant placement, because minimal bone is available for primary stabilization before this time. Further study is necessary to determine if the responses seen in this case are representative with use of a composite xenograft/autograft. Also, information is needed to ascertain the role of the autogenous bone graft material, and whether variation in the quantitative amount of each material may also alter the results. Finally, variables such as host response, graft materials utilized, technique employed, and skill of the operator may alter the results of the procedure. In this patient, the combination of a xenograft with autogenous bone from intraoral sources was histologicatly shown to convert to vital bone over a 12- to 20- month period. The replacement of the xenograft material is not a short-term event and, like nonvital human bone, takes close to 2 years to be replaced. Further research with a controlled method of measuring vital bone is indicated to determine the effect of known variables to optimize the success rate of this procedure. Acknowledgments The authors would like to thank Dr Victor Orlowski and Gloria Turner for their invaluable assistance in the preparation of the histoiogic material 1. Tatum H. Maxillary and Sinus implant reconstruction. Dent Clin North Am 1986.30:207-229. 2. Wood R, Moore D, Grafting of the maxillary sinus with intraorally harvested autogenous bone prior to implant placement. Int J Oral Maxillofac Implants 1988;3.209-214. 3. Small S. Zinner ID, Panno FV. Shapiro HJ. Stein Jl. Augmenting the maxillary sinus for implants; Report of 27 patients. Int J Oral Maxiliofac Implants 1993:8:523-528 4. Wetzel A, Stich H. Caffesse R. Bone apposition onto oral implants in fhe sinus area filled with different grafting materials. Clin Oral Implants Res 1995;6:155-163. 5. Jensen O. Guided bone graft augmentation. In: Buser D. Dahlin C, Schenk RK (eds). Guided Bone Regeneration in Implant Dentistry. Chicago: Quintessence, 1994: 235-264. 6. Boyne R James R. Grafting the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980:38: 613-616. 7. Moy P, Lundgren S. Holmes R. Maxillary sinus augmentation: Histomorphometric anaiysis. J Oral Maxillofac Surg 1992:51:857-862. 8. Cheung H, Tofe A. Mechanism of cell growth on calcium phosphate particles: Role of cell-mediated dissolution of calcium phosphate matrix. STP Pharma Sciences 1993; 3:51-55. 9. Salama R. Xenogeneic bone grafting in humans. Clin Orthop 1983:174: 113-121. Volume 16, Number 1, 1996