Implant Stability Measurements Using Resonance Frequency Analysis in the Grafted Maxilla: A Cross-Sectional Pilot Study

Lars Rasmusson, DDS, PhD;*t Goran Stegersjo, DDS;* Karl-Erik Kahnberg, DDS, PhD;* Lars Sennerby, DDS, PhDtS

ABSTRACT

Background: High failure rates have been presented for implants placed in grafted bone. The bone graft-implant interface constitutes a most complex healing situation, where the time scale for osseointegration and development of implant stability currently is not known. Purpose: The a m of the study was to measure the stability of implants placed in grafted bone after various follow-up periods. i
Methods: Implant stability measurements by means of resonance frequency analysis were performed in 10 patients previously ih treated w t a Le Fort I osteotomy and interpositional bone grafts. The implants were placed 3 to 4 months after the grafting procedure. Sixty-seven Branemark implants were subjected to resonance frequency analysis measurements at fixture placement and up to 5.5 years after implant surgery. Periapical radiographs were used for assessment of margmal bone levels.

Results: The radiographic examinations showed marginal bone loss with time during the 5.5-year follow-up. The resonance frequencies varied from 5860 to 8440 Hz. When accounting for abutment length and marginal bone level, there was a tendency of increasing resonance frequency with time. Two implants with low resonance frequencies failed during the prosthetic phase. Conclusion: The results indicate an increased implant stability with time, which may reflect bone formation, remodeling, and maturation at the implant interface.
KEY WORDS: bone grafts, implant stability, Le Fort I osteotomy, resonance frequency analysis, titanium implants

rosthetic reconstruction of the severely resorbed maxilla using implants often requires autogenous bone grafting to increase the load-bearing bone volume. The bone graft-implant interface constitutes a complex healing situation and involves revascularization and incorporation of the grafts as well as integration of the implants. The optimal timing for placement of implants in grafted bone to achieve maximal stability currently is not known. Primary implant stability is achieved at implant placement surgery and is a result of the surgical technique, implant design, and mechanical

*Department of Oral and Maxillofacial Surgery, Brinemark Clinic, +Department of BiornateriaMHandicap Research, Goteborg University, and *Department of Oral Rehabilitation, Brinemark Clinic, Gothenburg, Sweden Reprint requests: Lars Rasmusson, DMD, PhD, Department of Oral and Maxillofacial Surgery, Goteborg University, Box 450, SE-405 30 Gothenburg, Sweden
01999 B.C. Decker Inc.
70

properties of the bone. Secondary implant stability also is determined by the result of the repair process initiated by the surgical preparation of the bone, that is, formation and maturation of the bone at the implant interface. Thus, the final implant stability is determined by mechanical properties and the healing capacity of the bone bed. Experimental investigations have demonstrated a better integration of implants in bone grafts if a delayed technique is used compared to simultaneous For instance, Ramusson et a1 showed a higher degree of bone-implant contact and stability for implants placed in onlay bone grafts after healing of the graft compared to a simultaneous approach in which implants and bone graft were placed in one session.2 Histology of titanium microimplants placed and retrieved from 10 patients treated with autogenous bone grafts showed more bone when a delayed approach was used.3 It was speculated that the favorable results were achieved because the delayed implants were placed

RFA of Implant Stability in Grafted Maxillae 71

in revascularized bone and the surgical trauma initiated a repair process similar to that in normal bone. From the literature, it is clear that there are biologic advantages when using a delayed approach, as more bone is found at the implant interface. Thus, it can be anticipated that delayed implant placement will reach a higher degree of stability in a shorter period of time than simultaneously placed implants. However, the clinical documentation is not conclusive at this time.435 Registration of implant loss is important when reporting the clinical outcome of grafting procedures. The resonance frequency analysis (RFA) technique has been proven to be sensitive in monitoring changes in implant ~tability.~-~ this technique the resonance With frequency (RF) of a transducer that is attached to the implant is measured. The RF is determined by the stiffness of the bone-implant complex and is influenced by ~>~ abutment height and marginal bone ~ O S S . This technique might be useful in the study of the behavior of implants placed in grafted bone. The purpose of the present clinical pilot study was to measure implant stability in 10 patients treated with Le Fort I osteotomy and interpositional bone grafts and delayed implant placement.
MATERIALS AND METHODS

level. The radiographs were put on a light box and were captured by a charge coupled device (CCD) camera. The images were stored in a personal computer (PC) with a picture analyzing system. Contrast and light were automatically optimized whereafter the marginal bone level related to the reference point was measured on the mesial and distal aspect of each implant.1 A mean value was calculated for each implant.
Resonance Frequency Analysis

Resonance frequency analysis according to Meredith and co-workers2 was used for stability measurements at implant placement surgery (1 patient), at abutment connection 6 months later (1 patient), and 1 year (3 patients), 1.5 years (2 patients), 3.5 years (1 patient), 4.5 years (1 patient), and 5.5 years ( 1 patient) after implant placement. The testing equipment comprised a frequency response analyser, a PC, dedicated software, and transducers for connection to implant and abutment. Fixed prostheses were removed prior to testing. All abutment screws were tightened prior to the measurements. A transducer was attached to the furtures or abutments

Subjects

Ten patients (2 male; 8 female) with severe maxillary atrophy were subjected to Le Fort I osteotomy and interpositional bone grafting and delayed placement of titanium implants (Brhemark System, Nobel Biocare AB, Gothenburg, Sweden). Mean age was 62 years (range, 49-75 yr) at bone grafting surgery. Implant placement was performed 3 months after the grafting procedure. Abutment connection was performed 6 months after implant surgery.
implants and Abutments

Of 67 standard Briinemark System implants placed, six were subjected to RFA measurements on implant level and 61 on abutment level. Implant length ranged from 10 to 18 mm in length. Conical or standard abutments varied from 1 to 10 mm in length.
Radiography

Periapical radiographs taken at or close to the appointment for RFA were used to assess the marginal bone

Figure 1. Clinical photograph of the RFA transducer connected to an implant abutment in a maxilla that has been subjected to Le Fort I osteotomy and interpositional bone grafts.

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Clinical Implant Dentistry and Related Research, Volume I, Number 2, 1999

0
0

6
I

0 0

Time since implant placement (years)

Figure 2. Mean marginal bone levels for each patient by time since implant placement. (r = 0.59; p = ,096)

ginal bone resorption were accounted for. For this purpose, the transducers were calibrated using an implant embedded in plaster and abutments of different lengths. As previously reported, there was a linear relation between height above the bone crest and RF.6>7 The RFA measurements were easy and quick to perform. Less than 1 minute was used for attaching, measuring, and removing the transducer for each implant. No discomfort was reported from any patient except in one case with a mobile implant.
Statistics

with the use of a torque controller set at 10 ncm (Figure 1). The RF, recorded and automatically stored in the computer, was seen as a peak in a frequency-amplitude plot of the data and expressed in Hz. Since the RF in part is determined by the distance from the transducer to the first bone contact, abutment lengths and mar-

The Spearman correlation test was used for statistical analysis.

RES ULTS

4.0

6.0

8.0

10.0

12.0

14.0

Frequency (kHz)

The radiographic examinations showed marginal bone loss with time (r = 0 . 5 9 , ~ .096) (Figure 2). Resonance < frequencies from 5860 Hz to 8440 Hz were measured. When adjusting for abutment lengths and marginal bone loss, the calibrated RFs ranged from 6410 Hz to 9308 Hz. Implants with high RF showed distinct peaks when amplitude was plotted by frequency, whereas implants with a low RF generally showed broader and lower peaks (Figure 3). Although the single RFs varied, there was a tendency for increased stability with time when a mean value was calculated for each patient (r = 0.59, p < .072) (Figure 4). One implant with an extremely low RF at abutement connection failed during prosthetic treatment (see Figure 3, B). One clinically mobile implant showed double resonance peaks, the first at 6200 Hz and the second at 9620 Hz (Figure 5). This implant was later removed.
DISCUSSION

o.40

1
1

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6.0

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16.0

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Frequency (Wz)

Figure 3. Frequency-amplitude plot indicating A, successful integration as measured 6 months after implant placement, and B, low stability of the implant (first peak) as measured 6 months after implant placement. The implant failed during the prosthetic phase. The second peak corresponds to the second resonance normally not seen below 15 kHz.

The present pilot study using RFA for implant stability measurements in the grafted maxilla confirmed the reported clinical feasibility of the technique as shown for craniofacial implants and for oral implants placed in nongrafted b ~ n e . ~ - Within the limits of the present ~>' patient material and cross-sectional character of the study, results indicated an increase of implant stability with time that is in line with measurements on implants in normal bone.7 The increase probably reflected bone formation and maturation in the implant interface and indicates that the grafted maxilla has the capacity to integrate titanium implants. However, since no control group was used, it is not possible to directly compare the

RFA of Implant Stability in Grafted Maxillae

73

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a

&

8000
0

& 7400

8 7600

6000 4

-1
A

1 2 3 4 5 Time since implant placement (years)

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6
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-1

Time since implant placement (years)

Figure 4. Calibrated resonance frequencies by time for all implants (A) and calibrated mean resonance frequency for each patient by time ( B ) (r = 0 . 5 9 ; ~ .072). =

stability with that of implants in ungrafted bone. Neither is it possible to conclude whether the delayed technique results in a higher stability or in sufficient stability in shorter periods of time, compared to simultaneous graft and implant placement. For that purpose comparative longitudinal studies are needed. The RFA measurements correlated with clinical observations. Although all implants were found to be clinically stable in one patient, one of the implants showed a low RE This implant failed later during the prosthetic phase and was removed from the patient. One implant in a second patient was clearly rotationally mobile. The RFA showed double RFs, the first low one probably reflected the implant-bone stiffness, whereas the higher RF was the second mode, normally not seen below 15 kHz. This implant also had to be removed. Implant stability is determined by the biomechanical properties of the bone, the surgical technique, the implant design, and the healing capacity of the traumatized bone. As measured with RFA, implant stability is determined by the stiffness of the interfacial bone, which varies owing to type of bone (i.e., the cortical: trabecular bone r a t i ~ )In~viable bone it also depends on the time . of healing, since bone forms and condenses toward the implant surface and reaches a higher stiffness with time as a result of the maturation p r o ~ e s s .The grafted max~.~ illa constitutes a complex biomechanical and healing situation. The stiffness of the bone surrounding the implants depends on the properties of both the grafted and recipient bone. Initially the grafted and the recipient bone will not react as a homogeneous structure. Moreover, depending on when implants are placed, the healing capacities of grafted and recipient bone are different.

It may be anticipated that the grafting technique reported in the present study (i.e., Le Fort I osteotomy and interpositional bone grafting) is favorable from both biomechanical and a healing perspective. With this technique the grafted bone is placed between viable recipient bone. Theoretically, from a lateral aspect, the implants will be surrounded by homogeneous bone structures at different levels. This may be beneficial for the ability of the implants to withstand bending loads. Friberg and co-workers showed, in a longitudinal study using RFA of maxillary implants, that stability was increased up to 20 months post~peratively.~ results The are in accordance with the theory that bone formation and maturation may take up to 12 to 18 months.12J3 Moreover, in the grafted situation, as studied in the present investigation, the healing period may be 2 years or

o.80i
I
I I

4.0

6.0

1. 00 Frequency (kHz)

SlO

li.0

14.0

Figure 5. Frequency by amplitude plot for a mobile implant 1.5 years after implant placement. Double peaks are seen, the first at 6200 Hz and the second at 9620 Hz. The first is the primary natural frequency and the second is attributable to an asymmetry, owing to the mobility of the implant.

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Clinical Implant Dentistry and Related Research, Volume 1 , Number 2, 1999

5. Donovan MG, Dickerson NC, Hanson LJ, Gustafson RB. Maxillary and mandibular reconstruction using calvarial bone grafts and Brinemark implants. A preliminary report. J Oral Maxillofac Surg 1994; 54:588-594. 6. Meredith N, AUeyne D, Cawley P. Quantitative determination of the stability of the implant-tissue interface using resonance frequency analysis. Clin Oral Implant Res 1996; 7: 261-267. 7. Meredith N, Book K, Friberg B, Jemt T, Sennerby L. Resonance frequency measurements of implant stability in vivo. A cross-sectional and longitudinal study of resonance frequency measurements on implants in the edentulous and partially dentate maxilla. Clin Oral Implant Res 1997; 8: 226-233. 8. Friberg B, Sennerby L, Linden B, Grondahl K, Lekholm U. Stability measurements of one-stage Brinemark implants during healing in mandibles. A clinical resonance frequency study. Int J Oral Maxillofac Surg 1999; 28:266-272. 9. Friberg B, Sennerby L, Meredith N, Lekholm U. A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20 month clinical study. Int J Oral Maxillofac Surg 1999; 28:297-303. 10. Hollender L, Rockler B. Radiographic evaluation of osseointegrated implants in the jaws. Dentomaxillofac Radio1 1980; 9~91-95. 11. Heo SJ, Sennerby L, Odersjo M, et al. Stability measurements of craniofacial implants by means of resonance frequency analysis. A clinical pilot study. J Laryngol Otol 1998; 112~537-542. 12. Brinemark P-I, Hansson BO, Adell R, et al. Osseointegrated implants in treatment of the edentulous jaw. Experience from a 10-year period. Stockholm: Almquist & Wiksell, 1977. 13. Roberts E, Garetto L, Brezniak N. Bone physiology and metabolism. In: Misch C, ed. Contemporary implant dentistry. St. Louis: Mosby Year Book, 1994:327-368. 14. Burchard H. The biology of bone graft repair. Clin Orthop 1988; 174:28-42. 15. Isaksson S. Evaluation of three bone grafting techniques for severely resorbed maxillae in conjunction with immediate endosseous implants. Int J Oral Maxillofac Implants 1994; 9~679-688. 16. Kahnberg KE, Nilsson P, Rasmusson L. Le Fort I osteotomy with interpositional bone grafts and implants for rehabilitation of the severely resorbed maxilla. Int J Oral Maxillofac Implants (In press). 17. Nystrom E, Lundgren S, Gunne J, Nilson H. Interpositional bone grafting and Le Fort I osteotomy for reconstruction of the atrophic edentulous maxilla. Int J Oral Maxillofac Surg 1997; 26:423-427.

10nger.l~Within the limits of the present study, results indicated an increase in stability up to 4 years after implant placement. Therefore, the high failure rate reported for soft bone qualities and grafting procedures may, from a biologic perspective, be attributable to too short healing periods. The clinical documentation of the Le Fort I osteotomy and bone grafting technique indicate better results if a delayed technique is used and if a long primary healing period of the bone graft is allowed prior to implant placement. Isaksson reported loss of 13 of 41 implants (31.7%) when using simultaneous placement of im~1ants.l~ Recently, Kahnberg and co-workers lost 15% of implants using 3 months of primary healing of the bone grafts and delayed implant placement.16 Nystrom and co-workers17also used a two-stage approach with a healing period of 6 months for the graft and lost 3 of 60 implants (5%) during a 15- to 39-month follow-up. It is concluded that RFA may serve as a sensitive tool for monitoring changes in clinical implant stability in the follow-up of patients with grafts. Results from this cross-sectional pilot study suggest an increase of implant stability with time. However, longitudinal studies are needed to further follow the development of stability and the behavior during loading of implants in grafted bone.

REFERENCES
Shirota T, Ohno K, Michi KI, Tachikawa T. An experimental study of healing around hydroxylapatite implants installed with autogenous iliac bone grafts for jaw reconstruction. J Oral Maxillofac Surg 1991; 49:1310-1315. Rasmusson L, Meredith N, Cho IH, Sennerby L. The influence of simultaneous vs. delayed placement on the stability of titanium implants in onlay bone grafts. A histologic and biomechanic study in the rabbit. Int J Oral Maxillofac Surg 1999; 28:224-231. Lundgren S, Rasmusson L, Sjostrom M, Sennerby L. Simultaneous or delayed placement of titanium implants in free autogenous iliac bone grafts. Histological analysis of the bone graft-titanium interface in 10 consecutive patients. Int J Oral Maxillofac Surg 1999; 28:31-37. Schliephake H, Neukam FW, Wichmann M, Hausamen JE. Langzeitergebnisse osteointegrierter Schraubenimplantate in Kombination mit Osteoplastiken. Z Zahnartzl Implant01 1997; 13:73-78.