Choice of Graft Material in Relation to Maxillary Sinus Width in Internal Sinus Floor Augmentation

J Oral Maxillofac Surg 68:1859-1868, 2010

Choice of Graft Material in Relation to Maxillary Sinus Width in Internal Sinus Floor Augmentation Ho-Yeol Jang, DDS,* Hyoun-Chull Kim, DDS, PhD,† Sang-Chull Lee, DDS, PhD,‡ and Jang-Yeol Lee, DDS§ Purpose: When grafts with solely osteoinductive or osteoconductive effects are used in the maxillary sinus,

the medial wall of the sinus membrane should be reflected to receive the vascular supply and the osteoconductive effect. Because the internal sinus floor augmentation is a blind technique, it is impossible to directly verify whether the medial sinus wall is reflected in the operation. The purpose of this study is to describe the modality of choice among the grafting materials and techniques in relation to the width of the maxillary sinus through preoperative planning and measuring in computed tomography (CT) images. Patients and Methods: In a total of 57 patients, 100 implants were placed by 3 different sinus floor augmentation techniques. Postoperative cone-beam CT (CBCT) scans were performed and the arrival distance of grafts from lateral wall to medial wall at the apical end level of the implant in the maxillary sinus was measured. Results: Buccolingual arrival distances of grafts were measured to be a mean of 12.1 mm ⫾ 2.0 in postoperative CT images. In 23 of 77 cases (29.9%) in which distances were greater than 12.1 mm, the grafts made contact with the medial wall. However, in 22 of 23 cases (95.7%) in which distances were less than 12.1 mm, the grafts made complete contact with the medial wall. Conclusions: The buccolingual width of the maxillary sinus should be measured at the apical end level of the implant that will be placed in preoperative CT. In the internal sinus floor augmentation, grafting materials with solely osteoconductive potential are to be used for narrow sinuses. For large sinuses, autogenous bone with osteogenic potential should be used; alternatively, the reflection of the medial wall by the lateral window technique is recommended. Crown Copyright © 2010 Published by Elsevier Inc on behalf of the American Association of Oral and Maxillofacial Surgeons. All rights reserved. J Oral Maxillofac Surg 68:1859-1868, 2010 Alveolar bone resorption and pneumatization of the maxillary sinus after the extraction of teeth limits the quantity and quality of the bone necessary for successful implant placement, especially in the edentulous posterior maxilla.1 Many authors who have managed the insufficient bone problem in the posterior maxilla have reported various maxillary sinus floor augmentation techniques to increase bone volume and height. The sinus elevation surgery for implant placement was initially introduced by Boyne and James2 and by Received from LivingWell Dental Hospital, Koyang-City, Korea. *Resident, Department of Oral and Maxillofacial Surgery. †Oral and Maxillofacial Surgeon, Department of Oral and Maxillofacial Surgery. ‡Oral and Maxillofacial Surgeon, Department of Oral and Maxillofacial Surgery. §Oral and Maxillofacial Radiologist, Department of Oral and Maxillofacial Radiology.

Tatum.3 In these reports, the sinus was exposed by a modified Caldwell-Luc operation. A bony window was created in the lateral maxillary wall, and the sinus membrane was carefully reflected across the sinus floor and superiorly up the medial sinus wall. The grafts were placed on the bony cavity before the implant placement. Since these early reports, several modifications for the sinus floor elevation have been made to the surgical technique and in the materials used. A less invasive technique for the sinus floor elevation with grafting and simultaneous implant Address correspondence and reprint requests to Dr Jang: Department of Oral and Maxillofacial Surgery, LivingWell Dental Hospital, 110, Koyang-City, Korea; e-mail: [email protected] Crown Copyright © 2010 Published by Elsevier Inc on behalf of the American Association of Oral and Maxillofacial Surgeons. All rights reserved. 0278-2391/10/6808-0023$36.00/0 doi:10.1016/j.joms.2009.09.093

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Table 1. STUDY PATIENTS

No. of patients (n) Male/female (n) Mean age and range (yrs) Total No. of implants placed (n)

54 41/13 48.6, 19 to 74 100 (P2, 10; M1, 51; M2, 39)

Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

placement was introduced by Summers.4 It was described that the pressure from the shaved bone, the added graft materials, and the trapped fluids caused a dome-shaped elevation of the sinus floor as the osteotomes were inserted. Various internal sinus floor elevation techniques used to access the sinus cavity have also been developed, such as crestal core elevation,5 localized management of the sinus floor,6 antral membrane balloon elevation,7 the hydraulic sinus condensing technique,8 on-site sinus compaction,9 and the sinus drill technique.10 These techniques are simpler and less invasive compared with lateral approach techniques. To augment in the elevated sinus, various grafting materials have been used, including autografts, demineralized or mineralized allografts, xenografts, and alloplasts. These grafts have osteogenetic, osteoinductive, or osteoconductive potential that contributes to the formation of new bone. When grafts with solely osteoinductive or osteoconductive effects are used in the maxillary sinus, the medial wall of the sinus membrane should be reflected to receive the vascular supply and the osteoconductive effect.11 Because the internal sinus floor augmentation is a blind technique, it is impossible to directly verify whether the medial sinus wall is reflected in the operation. When the width of the maxillary sinus is wider, the force of the instrument acting on the reflection of the medial sinus wall in the alveolar crest is limited and the medial sinus wall cannot always be reflected. Therefore, when the width of the maxillary sinus is wider, the clinician should take these factors into consideration. To our knowledge, there are no published reports about whether reflection of the medial sinus wall and

the grafts that come into contact with the medial sinus wall occurs because of the various sinus floor augmentation techniques. The purpose of this study is to provide the modality of choice among the grafting materials and the techniques in relation to the width of the maxillary sinus through the preoperative planning and measuring in CT images for sinus floor augmentation.

Patients and Methods PATIENTS

A total of 54 partially or completely edentulous patients (41 men and 13 women, mean age 48.6 ⫾ 11.4 yrs, range 19 to 74 yrs) with atrophic posterior maxillas were selected for this retrospective clinical study. Patients were excluded if they exhibited pathological findings or had a history of maxillary sinus disease or operations. All participating subjects required sinus floor augmentation because of advanced resorption of the posterior maxilla and were examined by cone-beam computed tomography (CBCT, I-CAT; Imaging Sciences International, Hatfield, PA). A total of 100 implants were planned on 10 sites of the maxillary second premolar, 51 sites of the maxillary first molar, and 39 sites of the maxillary second molar (Table 1). GRAFTS

Two different types of grafts were used: 100% autogenous bone or composite grafts of more than 50% autogenous bone and the alloplast (Cerasorb; Curasan AG, Kleinostheim, Germany). The autogenous bone was harvested from the mandibular ramus or the iliac crest. All grafts were mixed with plateletrich plasma (PRP) before grafting. IMPLANT TYPES

Hydroxyapatite (HA)-coated implants (TSV; 13 mm length and 3.7, 4.7, or 6.0 mm diameter; Zimmer Dental, Carlsbad, CA) or the vacuum titanium plasma spray (VTPS)-coated implants (Pitt-Easy; 12 or 14 mm length and 3.25, 4.0, or 4.9 mm diameter; Sybron Implant Solutions, Orange, CA) were used throughout the study.

Table 2. DIFFERENCES RELATING TO IMPLANT SITES IN CBCT ANALYSIS

Implant Sites

n

Mean of Maxillary Sinus Width (mm)

Mean of Graft Arrival Distance (mm)

Contacted Site With Medial Wall

Second premolar First molar Second molar Total

10 51 39 100

12.7 ⫾ 4.0 15.2 ⫾ 3.7 14.4 ⫾ 4.0 14.6 ⫾ 3.9

10.6 ⫾ 2.5 12.3 ⫾ 1.8 12.2 ⫾ 2.0 12.1 ⫾ 2.0

7/10 (70%) 18/51 (35.3%) 20/39 (51.3%) 45/100 (45%)

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Table 3. DIFFERENCES REGARDING SURGICAL METHODS IN CBCT ANALYSIS

Surgical Method

n

Mean Maxillary Sinus Width (mm)

Mean Graft Arrival Distance (mm)

Contact With Medial Wall

Lateral approach technique Osteotome technique Sinus drill and osteotome technique Total

70 17 13 100

15.2 ⫾ 4.1 13.7 ⫾ 3.6 12.6 ⫾ 2.2 14.6 ⫾ 3.9

12.6 ⫾ 1.9 10.3 ⫾ 1.9 11.6 ⫾ 1.7 12.1 ⫾ 2.0

24/70 (34.3%) 9/17 (52.9%) 12/13 (92.3%) 45/100 (45%)

Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

SURGICAL TECHNIQUES

Sinus floor augmentation and the simultaneous implantation were carried out under local anesthesia using 1 of 3 surgical techniques: the lateral approach technique in 70 sites, the osteotome technique in 17 sites, and the crestal approach using sinus drills and osteotomes in 13 sites. The lateral approach technique was performed using a modified Caldwell-Luc procedure described by Kent and Block.12 The full-thickness mucoperiosteal flap was raised to expose the lateral wall of the maxillary sinus. The osteotomy of the lateral wall was performed using either a round diamond or carbide at a low speed, the piezoelectric device, or the Erbium laser (Fig 1). At this point, the bony window was completely removed (Fig 2). To create room for the grafts, the sinus membrane was gently reflected across the sinus floor (Fig 3). However, unlike in conventional techniques, the medial wall was not reflected (Fig 4). Grafts were pushed and packed layer by layer through prepared sites by using the osteotome technique (Figs 5, 6). The implants were placed simultaneously, and the grafts were condensed around the implant body through the lateral window. After filling the bony cavity completely, the bony window was repositioned to its original position (Fig 7). The osteotome technique was performed by a crestal approach and was reflected in a full-thickness mucoperiosteal flap to expose the crestal part of the alveolar ridge. After preparing the implant site with implant drills to 2 mm beneath the sinus floor, the

osteotomes were inserted to expand the preparation area both horizontally and vertically (Fig 8). Osteotomes in increasing diameters were used to create a site for implant placement and to elevate the sinus floor (Fig 9). Grafts were incrementally placed and packed into the prepared sites by osteotomes. The implants were placed simultaneously in the surgical sites. The sinus drill technique was performed in combination with the osteotome technique. It was reflected in the full-thickness mucoperiosteal flap to expose the crestal part of the alveolar ridge, similar to the osteotome technique. After preparation of the implant site with the implant drills to 1 mm beneath the sinus floor (Fig 10), sinus drills were passed to cut and elevate the cortical bone of the sinus floor. Sinus drills and osteotomes in increasing diameters were used to create a site for the implant placement and elevate the sinus floor (Fig 11). Grafts were incrementally placed and condensed into the prepared sites by condensers and osteotomes (Fig 12). The implants were placed simultaneously in the surgical sites. POSTOPERATIVE CARE

For all patients, the antibiotic Augmentin (375 mg, 3 times daily; GlaxoSmithKline, London, UK) was prescribed for 3 to 4 days following surgery. Patients were also given analgesics to control pain or discomfort. Then, 3 to 8 months afterward, the implants were loaded with single-tooth restorations, multipleunit implant-supported restorations, or overdentures.

Table 4. DIFFERENCES IN WIDTH OF MAXILLARY SINUS IN CBCT ANALYSIS

Maxillary Sinus Width Large sinus ⬎12.1 mm ⱖ16.0 mm (max) Narrow sinus ⱕ12.1 mm ⱕ11.3 mm (min)

n

Mean Maxillary Sinus Width (mm)

Mean Graft Arrival Distance (mm)

Contact With Medial Wall

77 33

15.9 ⫾ 3.4 18.9 ⫾ 3.2

12.6 ⫾ 1.8 13.1 ⫾ 2.3

23/77 (29.9%) 0/33 (0%)

23 20

10.3 ⫾ 1.4 10.0 ⫾ 1.4

10.2 ⫾ 1.4 10.0 ⫾ 1.4

22/23 (95.7%) 20/20 (100%)

Abbreviations: max, maximum; min, minimum. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

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FIGURE 1. Osteotomy of lateral wall. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

Patients were followed up every 4 months for supportive care and evaluation. RADIOGRAPHIC ANALYSIS

Postoperative CBCT scans were taken the day after surgery for all patients and were analyzed with image reformatting software (SimPlant; Materialise, Leuven, Belgium). The augmented sites were measured along the buccolingual width of the maxillary sinus and the arrival distances of the grafts from the lateral wall to the medial wall at the apical end level of the implant in the maxillary sinus. Also recorded was whether the grafts came in contact with the medial wall (Fig 13).

FIGURE 3. Reflection of sinus membrane by hand instrument. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

nuses were observed. The maxillary sinus widths were measured as a mean of 14.6 ⫾ 3.9 mm (range, 6.0 to 27.6 mm) in the postoperative CT images: 12.7 ⫾ 4.0 mm at the second premolar, 15.2 ⫾ 3.7 mm at the first molar, and 14.4 ⫾ 4.0 mm at the second molar, respectively. The buccolingual arrival distances of the grafts were measured as a mean of 12.1 ⫾ 2.0 mm (range, 6.0 to 16.4 mm): 10.6 ⫾ 2.5 mm at the second premolar, 12.3 ⫾ 1.8 mm at the first molar, and 12.2 ⫾ 2.0 mm at the second molar, respectively (Table 2). In 45 sites (45%), the grafts came into complete contact with the medial wall (Tables 2, 3). The rate of contact with the medial wall tended to increase in the nar-

Results The 100 dental implants were placed in the grafted sinuses. No postoperative complications in the si-

FIGURE 2. Removal of lateral window.

FIGURE 4. Schematic drawing depicting minimal reflection of the sinus membrane except for the medial wall.

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FIGURE 5. Preparing of implant site by use of the osteotome technique. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

rower maxillary sinus (Tables 2, 3). The rate of the grafts that came into contact with the medial wall was calculated based on the mean arrival distance (12.1 mm; Table 4). In the 23 of 72 sites (29.9%) that were greater than 12.1 mm, the grafts made contact with the medial wall (Fig 14). In the 22 of 23 sites (95.7%) that were less than 12.1 mm, the grafts made complete contact with the medial wall (Fig 15). The grafts in 33 sites greater than 16.0 mm did not make complete contact with the medial wall, but the grafts in 20 sites less than 11.3 mm made complete contact with the medial wall (Table 4).

Discussion Currently, various sinus floor augmentation techniques and the use of various grafting materials have

FIGURE 7. Reposition of bony window. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

yielded a predictable and successful procedure for implant placement in the severely atrophic posterior maxilla.13-21 In addition, various grafting materials can be used for sinus floor augmentation. For successful sinus floor augmentation, the properties and requirements of the grafts in the augmented sinus should be considered. The maxillary sinus offers an isolated environment because the graft is in contact with the sinus bony walls and is not exposed to the oral cavity, which provides an excellent healing potential. It may be that the graft serves primarily as a space maintainer, which prevents the elevated sinus membrane from collapsing, and through its osteoconductive properties allows osteogenic cells from the bony sinus walls to migrate into the graft and to replace it with new bone.22 The grafting materials can be categorized into 4 groups: autografts, demineralized or mineralized allografts, xenografts, and alloplasts. Ideal grafting mate-

FIGURE 6. Packing and condensing of graft by use of the osteotome technique.

FIGURE 8. Horizontal and vertical expansion by osteotomes.

Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

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FIGURE 9. Osteotomes in increasing diameters. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

FIGURE 11. Elevation of sinus floor using sinus drill. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

rials should meet a number of requirements: osteogenetic (stimulate surviving osteoblasts to form new bone), osteoconductive (serve as a scaffold for the ingrowth of vessels from neighboring bone), and osteoinductive (make pluripotential mesenchymal cells differentiate into osteoblasts) effect.23 Autogenous grafts meet all of these requirements and have therefore been defined as the “gold standard” among grafting materials. Common donor sites are the mandible, iliac crest, tibia, and skull.24,25 Autogenous grafts provide an excellent source of cells, growth factors, and bone morphogenic proteins, with no risk of antigenicity or cross infection. The disadvantages of autogenous grafts include hospitalization (extraoral) or requirement of a second surgical site (intraoral), which increases the length of time of the surgery, the surgical risk, and the morbidity associ-

ated with the procedure.11 Because donor sites generally provide only a limited amount of grafts, autogenous bone is often mixed with other grafting materials (allograft, xenograft, or alloplast). The proportion of autogenous bone and other grafting materials is mainly dependent on the available quantity of autogenous bone. A higher proportion of autogenous bone improves osteogenic potential in the graft mixture. However, the ideal proportion of autogenous bone and other grafting materials is yet to be determined.26,27 Allografts can be cortical or trabecular and are harvested from deceased human donors. They are available in a freeze-dried form, eliminating the risk of cross-infection by processing and sterilization meth-

FIGURE 10. Prepared implant site with the implant drills.

FIGURE 12. Incremental placement and condensing of graft into prepared site.

Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

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FIGURE 13. Postoperative measuring in CBCT. a, width of maxillary sinus. b, arrival distances of the grafts from the lateral wall to the medial wall at the apical end level of the implant in the maxillary sinus. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

ods. Allografts can be mineralized or demineralized. Both forms have osteoconductive properties and can serve as a scaffold that promotes the growth of new bone. The osteoinductive ability of demineralized freeze-dried bone allograft is still questionable.28,29 Xenografts, particularly derived from bovine bone, act as a resorbable osteoconductive material in the augmented sinus.30 Osteoconductive properties of the xenografts may be documented by close contact between the grafts and newly formed bone.31,32 As xenografts have a relatively long resorption time, the graft particles are still present after 4 years in the present human specimens.33

Alloplast is the mineral or inorganic component of bone such as ␤-tricalcium phosphate, coral hydroxyapatite, or bioactive glasses. Hydroxyapatite is nonresorbable and acts as a scaffold for osteoconduction. In contrast, ␤-TCP is almost resorbed completely and replaced with new bone.34-38 Although the alloplast lacks growth factors, it does have osteoconductive properties. Generally, in sinus floor augmentation, resorption and replacement of the grafts initially occur by cells originating from the peripheral area of the graft.22 A proper reflection of the sinus membrane must include elevating the membrane from the medial wall of the sinus. This provides the blood supply to the graft, which comes from the bony walls of the sinus, allowing a more rapid formation of vital bone and a reduction of the time necessary for graft maturation.11 The volume of augmented graft is usually proportional to the size of the sinus. The time required for graft resorption and replacement by new bone is longer in a larger sinus. Therefore, the high osteogenic potential of autogenous bone is essential when the sinus floor augmentation is performed in a large sinus.22 The lateral window technique is a more invasive procedure than internal sinus floor augmentation, but the technique makes it possible to directly access and verify the medial sinus wall through a lateral opening. Although there are many reports39-45 denoting the high success rate of the internal sinus augmentations using allograft or xenograft, the study of verifying the reflection of the sinus medial wall as well as the resorption and replacement of the graft according to the width of the maxillary sinus is insufficient. If these problems undergo further research, the clinical success rate may be increased. Although there are no published reports, various clinical cases recently have reported that sinus floor augmentations using allograft or xenograft alone with

FIGURE 14. Graft without contact with medial wall in large sinus (red arrow). A, Preoperative cross-sectional image. B, Preoperative implant planning and measurement of sinus width. C, Postoperative measurement of buccolingual arrival distance of graft. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

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FIGURE 15. Graft contact with medial wall in narrow sinus (red arrow). A, Preoperative cross-sectional image. B, Preoperative implant planning and measurement of sinus width. C, Postoperative measurement of buccolingual arrival distance of graft. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

osteoconductive potential have failed, especially in the large maxillary sinus. In Figure 16, the “black hollow” appearance of the graft center is shown in the postoperative CT images of a patient who was referred to our hospital after sinus floor augmentation with xenograft in a large sinus. These radiolucent appearances could be speculated by the central area of grafts not being replaced with new bone, and changed with the granulomatic or necrotic tissues, evident by the fact that the grafts were not in contact with the medial wall and were too far from the medial wall to receive osteoconductive effect. In this study, the lateral approach techniques were modified from the conventional techniques. In the cases of the lateral approach, the osteotome was used to elevate the sinus membrane without the reflection of the medial sinus wall (Fig 4). Packing and condensing of the graft by using the osteotome technique can

FIGURE 16. “Black hollow” appearance of graft center in postoperative CT (red arrow). Case referred to authors’ hospital after sinus floor augmentation with xenograft in large sinus. Jang et al. Graft Material in Internal Sinus Floor Augmentation. J Oral Maxillofac Surg 2010.

cause the elevation of the sinus floor and the reflection of the medial wall, which is similar to the internal sinus floor augmentation (Figs 5, 6). This minimal reflection of the sinus membrane can be performed when autogenous bone with osteogenetic potential is used in the sinus grafting. The present study shows the significant relationship between the width of the maxillary sinus and the buccolingual arrival distance of the grafts in 3 different techniques of sinus floor augmentation (Tables 2-4). Physical pressure for the elevation of the sinus membrane is partially restricted when the width of the sinus is large, so the reflection of the medial sinus wall does not always occur in the internal sinus floor augmentations. In narrower sinuses, the elevation of the sinus floor and the reflection of the medial wall can occur simultaneously. In larger sinuses, however, it is difficult to induce a sufficient reflection of the medial wall. Therefore, if the grafts are not in contact with the medial sinus wall, the osteoconductive effect cannot contribute to form new bone. In conclusion, based on the results of this study, a mean arrival distance of grafts from the lateral wall to the medial wall can be used for the modality of choice among grafting materials in relation to the width of the maxillary sinus in the internal sinus floor augmentation. We observed that the measured buccolingual width of the maxillary sinus at the apical end level of the implant should be placed in preoperative CT image. The buccolingual arrival distances of the grafts were measured as means of 12.1 ⫾ 2.0 mm in the postoperative CT images. The rate of contact in contact with the medial sinus wall tended to increase in a narrower maxillary sinus. In a narrower sinus with a width of less than 12.1 mm, grafting materials with solely osteoconductive potential can be used in the sinus floor augmentation, as the osteoconductive effect from the medial wall is provided. In a larger sinus

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with a width greater than 12.1 mm, autogenous bone with osteogenic potential should be used. The reflection of the sinus medial wall by the lateral window technique is recommended if the autogenous bone cannot be used.

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