Localized sinus augmentation utilizing bone graft layering technique and implant placement : a retrospective 1-5 year clinical study

Introduction

Implant dentistry has become a well accepted component of dentistry, with favorable long term reports demonstrating the success of dental implants in fully and partially edentulous jaws. However, long term results of treatment to rehabilitate the edentulous posterior maxilla remains scarse and uncertain at times (^{Jaffin and Berman, 1991} ; ^{Nevins and Langer, 1993} ; ^{Bahat et al., 1993}).

Patients with edentulous posterior maxillae experience loss of alveolar bone and increased maxillary sinus. When the base of the maxillary sinus encroaches into the alveolar bone the condition is known as pneumatisation. Pneumatisation may expand well into the alveolar crest leaving minimal and at times no alveolar bone. The combined vertical atrophy and sinus pneumatisation often preclude the use of endosseous implants in this region. As a result of the loss of alveolar bone and increased maxillary sinus, augmentation techniques have been developed (^{Boyne and James, 1980} ; ^{Tatum, 1986} ; ^{Smiler and Holmes, 1987} ; ^{Kent and Block, 1989}).

Augmentation and reconstruction techniques have focused on obtaining vertical and buccal expansion. In order to achieve the reconstructive goals, certain procedures have been attempted including : onlay grafts harvested from rib, iliac crest, and intra-oral sites (^{Tolman, 1995}). Le Fort I osteotomy with inter-positional bone grafting combined with sinus augmentations have also been utilized. An obstacle to desired results has been that the procedures limit interocclusal space creating restorative difficulties. To overcome the limited interocclusal space inlay-type augmentation procedures are utilized to gain vertical height without encroachment.

The sinus augmentation procedure begins by creating a window (antrostomy) which is a modification of the Caldwell-Luc procedure (^{Tatum, 1986}) to the lateral border of the maxilla. This window creates the access needed to displace the periosteum and the epithelial lining of the sinus allowing the placement of graft materials. Bone graft materials used for this procedure have varied from autologous, homologous, heterologeous, to alloplastic, and combinations thereof. ^{Table I} presents the advantages and the disadvantages of some of these augmentation materials.

Various donor sites have been explored, however, autogenous bone harvested from the hip has remained the « gold standard » for grafting materials (^{Raghoebar et al., 1997}). Another preferred site is the intra-oral location. This location has been shown to be effective and has advantages over the extra-oral site due to its close proximity to the recipient site, decreased healing periods, and decreased morbidity. The chin as an intra-oral donor site allows enough autogenous bone for a moderate to large unilateral sinus or a bilateral small to moderate sinus lift. But those cases requiring additional amounts of graftable material can include bone substitutes. These substitutes are utilized in combination with a modified procedure known as the layering technique. In the past, increasing donor bone volume would be met by mixing autogenous bone with bone substitutes. The new technique excludes the mixing of bone graft materials and allows autogenous bone to have maximal contact with implants while bone substitutes are used in the remote locations.

The timing of implant placement is predicated on the status of the alvelor bone volume. In the 1980's modifications regarding the timing of implant placement and sinus augmentation were discussed (^{Lundgren et al., 1996}). The modifications recommended employing an one stage approach or the two stage approach of bone reconstruction and implant placement.

Grafting of the resorbed maxilla can be done at the time of implant placement (one-stage approach) or prior to implant placement (two-stage approach). The placement of the implants can correspond with the sinus lift and placement of the graft material if there is at least 4 to 5 mm of bone height to allow primary implant stability and appropriate positioning of the implants. The simultaneous-placement procedure allows direct visualization of the implants and requires less healing time over a delayed placement (two stage) approach. If the thickness of the sinus floor is less than 4 mm it is preferable to augment the sinus floor and wait 6 to 9 months in order to let the augmented bone mature before implant placement (two-stage).

This study demonstrates the short to medium term results of simultaneous and delayed surgical techniques. These techniques for sinus floor grafting include utilization of particulated mandibular autograft, and/or a bone substitute used in conjunction with a layered technique (^{table II}).

Materials and methods

Twenty-eight patients (15 women, 13 men) were treated with sinus augmentation and dental implants. The mean age was 47 years (range 31-68 years). A total of 36 sinus augmentations were performed and 82 implants were placed. 70 implants were placed simultaneously (one stage) with the sinus augmentation and 12 implants were placed after the sinus was augmented (two stage). In 12 sinus augmentations autogenous bone harvested from the chin and/or the tuberosity area was used as graft material (chin-block in one of the cases and particulated bone graft in the other 11 cases). In 10 cases a combination of particulated autogenous bone and DFDB was used. In 3 cases the combination of a mono-cortical autogenous bone block from the chin and DFDB was used. In 10 cases a combination of particulated autogenous bone and Bio-Oss^® was used. In one case the combination of particulated autogenous bone and resorbable HA was used. The implants were all Brånemark type (standard titanium fixture) of varying sizes.

All the patients received prophylactic antibiotic treatment (1 000 mg amoxycilline) 1 hour prior to the surgery and continued the treatment (500 mg amoxycilline, 4 x a day) for at least one week after the surgery. Ibuprofen with or without codeine supplements was prescribed as pain medication and oral hygiene was maintained by chlorhexidine rinsing for 1 to 2 weeks following the procedure(s).

Treatment planning and patient selection

Prior to treatment, panographs and peri-apicals were used to evaluate the surgical sites and remaining alveolar bone. To evaluate the skeletal relationship and the bone graft harvesting sites, lateral cephalometrics were used. In extremely resorbed cases, a CT scan was required. Models were made of all patients.

The contra-indications for this therapy included smoking, chronic sinusitis (^{Timmenga et al., 1997}), radiation therapy, and diabetes.

Surgical procedure

Sinus augmentation and implant placement

Posterior superior maxillary, infraorbital, palatal block, and infiltration anesthesia (xylocaine 1/100,000) was administered to the patients. In some cases patients were given intravenous sedation. Incisions were made to allow adequate access of the anticipated antrostomy and implant osteotomies (^{fig. 1} and ²). The primary incision was made on the crest and included mesial and distal-buccal vertical-releasing incisions. A vertical releasing incision in the canine fossa allowed adequate access to the anticipated window site and allowed soft tissue closure over the implants and sinus window. A full thickness flap was then elevated superiorly to the level of the malar buttress allowing adequate exposure of the anticipated antrostomy. Trans-illumination of the sinus from the palate, and radiographs assisted with assessing the sinus floor boundaries and its anterior limit.

Once adequate access to the sinus cavity was achieved a lateral wall antrostomy was cut without tearing the antral mucosa using a small round diamond bur. The antrostomy is rectangler in shaped and 10 mm × 6 mm in most cases. The outline of the antrostomy is followed with the bur until a dark shadow is seen. This outlined lateral wall is removed or infractured and the Schneiderian membrane is elevated with the aid of curettes and sinus elevators (ESIM1, Imp Jo/6, Imp Jo/7 ; Hu-Friedy, Chicago, IL). Small tears in the membrane can occur during elevation and be corrected if it extends beyond the torn boundary. Collagen or polylactic acid membrane materials were used to cover any tear (Bio-gide, Geistlich ; Resolute, W.L. Gore & Associates).

Implant osteotomies were then prepared to allow placement of 3.75 mm to 5.0 mm diameter Branemark implants. After the implants sites were prepared, the harvesting procedure was started. For bone harvesting from the chin, an incision was made 10 mm below the attached gingiva level from canine to canine revealing the bone (^{fig. 3}). The required amount of cortical bone was taken with a 6, 8, or 10 mm trephine drills (TREJO 9-11, Hu-Friedy, Chicago, IL). A collagen sponge was placed in the defect and the mental muscle was sutured with several internal mattress sutures (Vicryl 5-0, Ethicon). The incision was closed with continuous locking sutures (Vicryl 6-0, Ethicon). The harvested bone was particulated using the R. Quetin bone mill when indicated.

The sinus was packed with the autogenous bone alone or in combination with bone substitute utilizing the layering technique. If insufficient bone was present, the bone substitute of choice was condensed into the remote areas of the sinus and autogenous bone was placed into the anticipated position of the implant. The bone substitute was first placed in the anterior, medial and finally posterior locations provided that there still remained adequate room for implants and autogenous bone (^{fig. 4}).

Implants were placed before complete filling of the sinus. Finally, after implant placement the last layer of autogenous bone could be postitioned on the lateral borders of the implants. If more bone volume was needed on the lateral aspect then a final layer of bone subsitute was used.

The implants were placed using the bone condensation technique. Preparation utilizing smaller-sized osteotomies allows the implants to condense the adjacent bone providing greater bone density and greater implant stability. The stability of the implants was checked and if not achieved the implant was removed. The lateral wall can consist entirely of bone substitute in the areas remote to the implant site. Subsequently, a membrane (resorbable : 49.4 %, non-resorbable : 50.6 %) was placed over the sinus window and attached with titanium pins (IMZ membrane tacks, Friatec, Germany). The flap was closed with interrupted and mattress e-PTFE sutures (^{fig. 5}).

Abutment surgery

Abutment surgery was planned after a submerged healing period of 6 to 9 months without loading. A split thickness flap was elevated toward the buccal aspect to increase the quantity of the keratinized attached gingiva surrounding the implants (^{fig. 6} and ⁷). The cover screws were removed and the healing abutments were placed. The flap was closed with mattress and interrupted sutures. The soft tissue was left to heal undisturbed for approximately 4-6 weeks.

Prosthodontic restorations

All partially edentulous patients were treated with fixed bridgework after an appropriate healing period. Fully edentulous patients were treated with fixed or a removable prosthesis (^{fig. 8}, ⁹ and ¹⁰).

Results

Seventy-seven of the placed implants were successful at the time this article was written (93.9 %) and 5 implants (6.1 %) have failed (^{table III}). Implant mobility and/or advanced bone loss was considered the criteria for implant failure. Sinusitis due to the operation is considered as a complication but did not occur in any of the cases.

There was complete bone regeneration in all of the grafted sites. Short-term paresthesia occurred in some of the donor sites with no long-term effects.

The average length of loading was 20.01 months (with a range of 7 to 60 months). The length of placed implants ranged from 10 mm to 15 mm (average 13.7 mm). Implant width ranged from 3.75 mm to 5.0 mm. 72 implants were 3.75 mm in diameter, 9 implants were 4.0 mm, and 1 implant was 5.0 mm in diameter. The average crestal bone height was 4 mm, with a range of 1 mm to 10 mm (^{table V}).

The influence of the augmentation material (^{table III}), gender (^{table IV}), and remaining bone height (^{table V}) on the success of the treatment was also evaluated. The type of material used for the augmentation and the gender had little effect on the success of the treatment although particulated autogenous bone in combination with DFDB showed the highest survival rate (100 %) and autogenous block graft in combination with DFDB demonstrated the lowest survival rate (80 %). The survival rate of simultaneous implant placement, 95.5 %, versus delayed two-stage implant placement, 86.7 % is shown in ^{table VI} .

Discussion

The loss of dentition is usually accompanied by resorption of bone, and atrophied hard and soft tissues. Without reconstructive efforts specific to increasing bone volume implant placement may be compromised. The requirements for successful long-term implant treatment are predicated on adequate bone quality and quantity. The long-term success of loaded fixtures in reconstructive ridges or sinuses is still under investigation.

Brånemark demonstrated that implants can be a successful long-term treatment option for the edentulous patient. Recently, long term survival in partially edentulous patients has also been shown. In the partially edentulous cases, the maxillary posterior region has a lower implant success rate over all. The lower success rate is attributable to inadequate bone quality and quantity.

Inadequate bone quality, especially type IV bone, has been associated with increased implant failure (^{Jaffin and Berman, 1991} ; ^{van Steenberghe et al., 1990}). The maxillary posterior has a thin cortical region and a high volume of porous cancellous bone corresponding to type III and type IV bone. ^{Jaffin and Berman (1991)} reported a 44 % fixture loss in the maxilla and 37 % fixture loss in the posterior mandible in type IV bone. ^{van Steenberghe et al. (1990)} also reported a 22 % failure rate in type IV bone. Studies have shown that implants survive in grafted bone better than in non-grafted maxillary posterior region. Limited histologic studies have shown that the graft sites can have a greater bone density and implant contact over non-grafted posterior maxilla regions (^{Valentini et al., 1998}) and that within the grafted sites the process of remodeling continues over time (^{Lundgren et al., 1996}).

Another factor associated with implant failure is fixture size. Brånemark did his initial studies with 10 mm implants and his implant survival rate remains a standard. Smaller fixture sizes have been shown to increase implant failure rates. ^{van Steenberghe et al. (1990)} showed failure rates of 10.7 % for 7 mm, 5.9 % for 10 to 13 mm, and 0 % for 15 mm implant lengths. Complicating the rehabilitation of the partially edentulous posterior maxilla is alveolar bone atrophy. The alveolar bone in the posterior maxilla is doubly resorbed by crestal resorption and apical atrophy due to pneumatisation of the maxillary sinus. It is advisable to perform a reconstructive procedure if an implant of 10 mm or greater cannot be placed.

Reconstruction procedures utilize bone or bone substitutes. Autogenous bone has remained the « gold standard » for grafting materials. The autogenous grafts act as a scaffold by transfering living osteocytes, as well as calcified tissues. The grafts also to a small extent, act as a reservoir for growth factors, such as bone morphogenic protein, which induces osteogenesis, chemotaxis, cell proliferation, and cell differentiation.

But autografts must utilize a secondary site for donor material. At least one report showed a morbidity rate of 9 % with iliac crest bone as the donor site (infection, blood loss from arterial injury, nerve injury, functional deficit, short and long term pain) (^{Kalk et al., 1996}). Two reports indicated minimal morbidity and ample graft material for a unilateral augmentation with the use of the chin as the donor site (^{Hunt and Jovanovic, 1999} ; ^{Lundgren et al., 1996}). The rationale for the intra-oral donor site is its close proximity to the recipient site, decreased healing periods, and decreased morbidity.

The chin allows enough autogenous bone for a unilateral sinus lift. Additional bone can be harvested from other intra-oral sites such as the mandibular ramus. In the past, increasing donor-bone volume could be met by mixing autogenous bone with allograft materials. This paper reports on a new sinus lift procedure which utilizes a layered technique for placing bone with bone substitutes, as well as the associated early results using the procedure. If insufficient bone was present, then this technique utilized bone substitutes in remote locations while the autogenous bone was placed in the implant or anticipated implant locations. The layered technique has the added advantage of allowing autogenous bone to be placed adjacent to the implant.

As a comparison to our own results ^{Tong et al. (1998)} performed a meta-analysis on survival rates for implants placed in grafted maxillary sinuses. The review considered 10 studies which had at least 10 patients within the study, using the studies with root-form endosseous implants, with drop-out rates less than 5 %, patient follow-up no less than 6 months. This review showed a survival rate of autogenous bone alone to be 90 % and 94 % for the combination of hydroxyapatite and demineralized freeze-dried bone. Additionally, the authors concluded that the studies reviewed showed implant survival rates as similar for autogenous bone, HA/autogenous bone mix, HA/DFDB, and HA alone.

Of the 36 sinus procedures in this study, 12 were augmented without the addition of bone substitutes. The remaining 24 sinus procedures were augmented using the layered technique. The combined grafts achieved osseointegration prior to loading, and only 4 lost osseointegration during the loading period, yielding a 93 % survival rate overall (4 lost implants out of 60). This can be compared to the autogenous bone alone which had a survival rate of 95.5 % (1 lost implant out of 12). The combined procedure which yielded the least desireable results was the autogenous block and DFDB, success rate of 80 %.

The sinus lift procedure originally discussed as a two-stage method by Tatum in 1976, was a modification of the Caldwell-Luc procedure. This was later modified by ^{Kent and Block in 1989} to allow simultaneous implant placement. In this study, both delayed and simultaneous implant placements were utilized, based on sufficient bone height. Delayed procedures are utilized when implant stabilization is not achieved or when insufficient crestal bone exists : 15 implants were placed as a two-stage procedure consisting of 6 implants within pure autogenous bone and 9 implants within autogenous bone and DFDB. The survival rate for the two-stage approach was lower (86.7 %) than the one-stage approach (95.5 %). In the two-stage approach one patient accounted for two lost implants while three different patients lost one implant apiece in the one-stage approach. The survival rate of all the cases did show a dependency on beginning bone height : 100 % survival rate existed in 7 mm or greater residual crestal bone, while 92.3 % and 94.3 % for 4-6 mm and 0-3 mm residual crestal bone, respectively.

Conclusion

All of the 82 implants placed into augmented sinuses achieved osseointegration prior to loading, and only 5 lost osseointegration during the loading period, yielding a 93.9 % survival rate overall. This study and others have shown that bone grafting in the maxillary sinus has met with high initial success rates. The high success rates are largely related to the unique cavity of the maxillary sinus. This cavity is one that can achieve an isolated milieu for the graft materials. Although the preliminary results are promising it must be remembered that this procedure is relatively new and the long-term results are only 5 years in duration.

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