Journal of Oral Implantology The volume behavior of autogenous iliac bone grafts after sinus floor elevation - a clinical pilot study --Manuscript Draft-Manuscript Number:

AAID-JOI-D-13-00246R1

Full Title:

The volume behavior of autogenous iliac bone grafts after sinus floor elevation - a clinical pilot study

Short Title:

Volume behaviour of iliac crest grafts

Article Type:

Clinical Research

Keywords:

iliac crest graft; sinus lifting surgery; three-dimensional resorption; healing time

Corresponding Author:

Marcus Gerressen, MD, DMD, PhD Heinrich Braun Hospital, Location Zwickau Zwickau, Saxonia GERMANY

Corresponding Author Secondary Information: Corresponding Author's Institution:

Heinrich Braun Hospital, Location Zwickau

Corresponding Author's Secondary Institution: First Author:

Marcus Gerressen, MD, DMD, PhD

First Author Secondary Information: Order of Authors:

Marcus Gerressen, MD, DMD, PhD Dieter Riediger, MD, DMD, PhD Ralf-Dieter Hilgers, DSc, PhD Frank Hölzle, MD, DMD, PhD Nelson Noroozi, DMD, PhD Alireza Ghassemi, MD, DMD, PhD

Order of Authors Secondary Information: Abstract:

Iliac crest is still regarded as one of the most viable source of autogenous graft materials for extensive sinus floor elevation. Three-dimensional resorption behavior has to be taken into account in anticipation of the subsequent insertion of dental implants. We performed three-dimensional volume measurements of the inserted bone transplants in a total of 11 patients (6 female and 5 male, mean age 52.3 years) who underwent bilateral sinus floor elevation with autogenous iliac crest grafts. In order to determine the respective bone graft volumes, cone-beam-CT studies (CBCT) of the maxillary sinuses were carried out directly after the operation (T0), as well as three (T1) and six months (T2) postoperatively. The acquired DICOM data sets were evaluated using suitable analysis software. We evaluated statistical significance of graft volumes changes using a linear mixed model with the grouping factors for time, age, side and sex with a significance level of p=0.05. 38.9 % of the initial bone graft volume, which amounted to 4.2 cm3, was resorbed until the time T1. At the time T2, the average volume again decreased significantly by 18.9 % to finally reach 1.8 cm3. The results show neither age nor side dependency and apply equally to both genders. Without functional load, iliac bone grafts feature low volume stability in sinus augmentation surgery. Further clinical and animal studies should be accomplished to detect the optimal timing for implant placement.

Response to Reviewers:

At this point, we would like to thank the reviewers for their constructive criticism and the useful recommendations. The corresponding changes in the manuscript are

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highlighted in yellow. Reviewer #1: Abstract: -Suggest to replace this sentence as following,“iIiac crest is still regarded as one of the most viable source of autogenous graft materials for extensive sinus floor elevation,. Three-dimensional resorption behavior has to be taken into account. in anticipation of the subsequent insertion of dental implants,” → “For sinus floor elevation, autogenous bone especially from the iliac crest is still regarded as one of the most convenient graft materials. Regarding the subsequent insertion of dental implants, the three-dimensional resorption behavior has to be taken into account.” was replaced by: “Iliac crest is still regarded as one of the most viable source of autogenous graft materials for extensive sinus floor elevation. Threedimensional resorption behavior has to be taken into account in anticipation of the subsequent insertion of dental implants.” -Suggest to replace this sentence as following “We evaluated tatistical significance of graft volumes changes using a linear mixed model with the grouping factors for time, age, side and sex with a significance level of p=0.05.” → “The detected graft volumes were statistically evaluated by using a linear mixed model with the grouping factors time, age, side and sex with a significance level of p=0.05.” was revised to: ”We evaluated statistical significance of graft volumes changes using a linear mixed model with the grouping factors for time, age, side and sex with a significance level of p=0.05.”

-→ “38.9 % of the initial bone graft volume, which amounted to 4.2 cm3, were resorbed until…” was revised to:”38.9 % of the initial bone graft volume, which amounted to 4.2 cm3, was resorbed until…” -Suggest to replace with‘considered accordingly”→ “So, the healing time before implant insertion has to be reconsidered.” was revised to: ”Further clinical and animal studies should be accomplished to detect the optimal timing for implant placement.” Introduction: -suggest to replace with “Some” → corrected as recommended -This statement is not correct according to available literature. Based on available evidence and systematic reviews it is well accepted that the key factor for sinus elevation success is the space maintenance to lift of the sinus membrane not the choice of graft material→ Of course, you are right as far as the scientific background is concerned. However, here we would like to emphasize that in practice almost each surgeon trusts in his own graft material (composition) of choice. Therefore “The question about what graft material should be used for the sinus lifting procedure is, however, largely divisive.” was revised to: ”The question about what graft material should be used for the sinus lifting procedure is, in practice, largely divisive.” Materials and Methods: -Suggest to revised to “the maximum possible amount of cancellous bone was then collected using Volkmann's spoons of suitable size from the opened marrow spaces→ changed as proposed

-→ “In the cases (n = 8), in which advanced maxillary atrophy …” was revised to: ” In eight cases, in which advanced maxillary atrophy …” -→ “…according to the buccal or else crestal contour of the alveolar ridge.” was revised to:” …according to the buccal and/ or crestal contour of the alveolar ridge.” Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation

-→ “The remaining portions of the block graft or, respectively, in the cases without onlay grafting, the entire bone blocks…” was revised to:” The remaining portions of the block graft, and in the cases without onlay grafting, the entire bone blocks…” Results: -→ “Already at T1, all grafts presented themselves totally osseously integrated on the CBCT scans (Figure 7).” was revised to: ” Already at T1, all grafts were integrated to host bone on the CBCT scans (Figure 7).” Discussion: -→ “In order to minimize this effect, great importance was attached to…” was corrected to: ”In order to minimize this effect, great importance was extended to…” -→ the word “implantation” was respectively replaced by ”implant placement” -→ “Certainly, the lacking physiological load of the grafted bone is one major problem…” was revised into: ”Certainly, lack of physiological load of the grafted bone is one major problem…” -→ “…successfully applied for replacement of autogenous bone grafts.” was revised to: ” …successfully applied as a replacement of autogenous bone grafts.”

-Suggest to rewrite as “Different treatment options with each individual patient discussing risks and benefits of authogenous bone grafting versus the use of biomaterials on an individual basis.”→ “However, the surgeon is obliged to discuss the possible ways of treatment with the patient and to set the indications in favor of autogenous graft material on the one hand, and alloplastic or xenogenic graft material on the other hand, very carefully and individually.” was revised to: ” However, the surgeon is obliged to discuss different treatment options with each individual patient discussing risks and benefits of autogenous bone grafting versus the use of biomaterials on an individual basis.” -Suggest to change to “Surgical strategies must be considered to reduce resorption of the graft volume observed when using iliac autogenous bone”→ “Therefore, a healing time of six months until implant insertion is definitely too long. Strategies must be developed to preserve as much graft volume as possible.” was revised to: ” Surgical strategies must be considered to reduce resorption of the graft volume observed when using iliac autogenous bone.”

Reviewer #2: General concerns: -The authors' have also presented what looks like pilot data from a clinical prospective study → The title was changed into: “The volume behavior of autogenous iliac bone grafts after sinus floor elevation – a clinical pilot study” Abstract: -In the final two sentences of the Abstract, the authors’ mention that “iliac bone grafts feature low volume stability in sinus augmentation surgery and that the healing time before implant insertion has to be reconsidered”. It seems that the previous statement sounds generic; the authors’ are encouraged to include a statement indicating that further clinical studies (both animal and human) are needed in the future. This is critical in order to better understand the dynamic behavior of iliac crest bone grafts in surgical pre-operative sites→ “So, the healing time before implant insertion has to be reconsidered.” was revised to: Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation

”Further clinical and animal studies should be accomplished to detect the optimal timing for implant placement.” Materials and Methods / Discussion: -In the true sense, the only reliable technique that can be utilized to measure the threedimensional area of the grafted site is by re-entry surgically at a future date, although this is impractical and unethical. Further, there is not yet a single reliable method of the volume measurement of the grafted site that can be performed non-invasively that has been developed. It is unclear as to why the clinicians’ in this study chose to utilize the DICOM data to generate software model of the three-dimensional structures and instead not utilize the typically used Hounsfield scale. Was it only because they did not have access to a regular CBCT machine, the limitation of the software or due to another reason. Several other studies in the available literature utilize Hounsfield units, albeit this technique might also have certain limitations in terms of varying radiodensities of different anatomical areas. Although the authors have indicated that using DICOM data could be a potential drawback, could they comment about possible solutions to address the same. → To our knowledge, CBCT images are in general not calibrated in HU. With the applied method, the host bone and the grafted bone could be distinguished at T0, at T1 and T2 based on the visible grey shades. The height of the host bone was then considered during the segmentation procedure at T1 and T2. In this context the statement “this, of course, is a weakness of the investigation in hand” means that it would have been interesting how the bone density of the new bone is compared with the host bone; however, because of the reasons mentioned above we did not take the greyscales of our CBCT as values for bone density. We revised the regarding passage in the discussion chapter: ”this, of course, is a weakness of the investigation in hand that the chosen method does not allow a statement on the density of the remodeled bone graft compared to the host bone.” -In line 103, the authors’ mention that two separate clinicians performed the volumetric determinations and subsequently the mean value from both measurements was utilized for this study. This is a descriptive statistical analysis that can be useful to only a certain extent. Additionally, the scientific method of reporting such data will be to evaluate the kappa value (kappa statistics to determine inter-examiner variability which typically stands at an agreement of 80%; i.e., = 80% to be scientifically/statistically acceptable). Was there a specific reason as to why kappa statistical analysis was not utilized in this study? Was this statistical tool not utilized considering the small number (n) of patients studied in this project? The authors’ justification and comments regarding these previously mentioned statements might be useful to readers of the manuscript.→ The measurements of the two examiners differed from each other for maximum 13%. Because of the small sample size we refrained from calculating the kappa value upon the advice of our statistician, Prof. Hilgers. In order to make the reasoning comprehensible to the reader we adjusted the pertaining paragraph: “however, all definite measurements were performed by two experienced examiners after undertaking a rehearsal round, and there was a difference of less than 13 % between both volume determinations. Because of this, and the small sample size, we abstained from calculating the kappa value to determine inter-examiner variability.”

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Rebuttal Letter (for revisions) Click here to download Rebuttal Letter (for revisions): Revision Notes.doc

*Article File

Original Investigation

The volume behavior of autogenous iliac bone grafts after sinus floor elevation – a clinical pilot study

Authors: Marcus Gerressen 1, MD, DMD, PhD Dieter Riediger 2. MD, DMD, PhD Ralf-Dieter Hilgers 3, DSc, PhD Frank Hölzle 4, MD, DMD, PhD Nelson Noroozi 5, DMD, PhD Alireza Ghassemi 6, MD, DMD, PhD

1

Head of the Department of Oral, Maxillofacial and Plastic Facial Surgery, Heinrich Braun

Hospital, Location Zwickau, Karl-Keil-Str. 35, 08060 Zwickau, Germany and Department of Oral, Maxillofacial and Plastic Facial Surgery, University Hospital of the Aachen University (RWTH), Pauwelsstr.30, 52074 Aachen, Germany

2

Professor and former Chair, Department of Oral, Maxillofacial and Plastic Facial Surgery,

University Hospital of the Aachen University (RWTH), Pauwelsstr.30, 52074 Aachen, Germany

4

3

Professor and Chair, Institute of Medical Statistics, University Hospital of the Aachen

University (RWTH), Pauwelsstr.30, 52074 Aachen, Germany

4

Professor and Chair, Department of Oral, Maxillofacial and Plastic Facial Surgery,

University Hospital of the Aachen University (RWTH), Pauwelsstr.30, 52074 Aachen, Germany

5

Consultant, Department of Oral, Maxillofacial and Plastic Facial Surgery, Heinrich Braun

Hospital, Location Zwickau, Karl-Keil-Str. 35, 08060 Zwickau, Germany

6

Assistant Professor, Department of Oral, Maxillofacial and Plastic Facial Surgery,

University Hospital of the Aachen University (RWTH), Pauwelsstr.30, 52074 Aachen, Germany

Corresponding author: Priv.-Doz. Dr. Dr. Marcus Gerressen Department of Oral, Maxillofacial and Plastic Facial Surgery, Heinrich Braun Hospital, Location Zwickau, Karl-Keil-Str. 35, 08060 Zwickau, GERMANY phone: +49 375 51-4803 fax: +49 375 51- 1560 e-mail address: [email protected]

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ABSTRACT Iliac crest is still regarded as one of the most viable source of autogenous graft materials for extensive sinus floor elevation. Three-dimensional resorption behavior has to be taken into account in anticipation of the subsequent insertion of dental implants. We performed three-dimensional volume measurements of the inserted bone transplants in a total of 11 patients (6 female and 5 male, mean age 52.3 years) who underwent bilateral sinus floor elevation with autogenous iliac crest grafts. In order to determine the respective bone graft volumes, cone-beam-CT studies (CBCT) of the maxillary sinuses were carried out directly after the operation (T0), as well as three (T1) and six months (T2) postoperatively. The acquired DICOM data sets were evaluated using suitable analysis software. We evaluated statistical significance of graft volumes changes using a linear mixed model with the grouping factors for time, age, side and sex with a significance level of p=0.05. 38.9 % of the initial bone graft volume, which amounted to 4.2 cm3, was resorbed until the time T1. At the time T2, the average volume again decreased significantly by 18.9 % to finally reach 1.8 cm3. The results show neither age nor side dependency and apply equally to both genders. Without functional load, iliac bone grafts feature low volume stability in sinus augmentation surgery. Further clinical and animal studies should be accomplished to detect the optimal timing for implant placement.

Key Words: iliac crest graft; sinus lifting surgery; three-dimensional resorption; healing time

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INTRODUCTION Tooth loss in the posterior maxilla and the resulting alveolar ridge resorption often cause difficulties regarding the prosthetic restoration. Inadequate treatment results are increasingly leading to more patient requests for an implant-supported dental prosthesis.1-3 However, treating the edentulous maxilla with endosteal implants represents a distinct challenge. Due to the insufficient bone height and the poor bone quality caused by atrophy, the surgical conditions for primary insertion of implants are unsuitable in some cases. This is because in addition to the resorption of the alveolar ridge with a marked reduction of cancellous bone, the maxillary sinuses expand in a caudal direction.4-6 Among all treatment procedures that restore a sufficient bone height for surgical implantation, sinus floor elevation - as first described by Tatum at the Alabama Implant Congress in 1976 and published by Boyne and James in 1980 – is probably the most widely used and best-studied method, that is established today as a standard technique mastered and applied by many surgeons.7,8 The question about what graft material should be used for the sinus lifting procedure is, in practice, largely divisive. Therefore, numerous materials, including allografts, xenografts, alloplastic materials, composite grafts composed of different types of transplants and even tissue-engineered bone have been proposed and used up to date.9-14 Nevertheless, despite the outstanding treatment results with bone substitute materials, autogenous bone is still a proven and frequently applied graft material.9,15-21 This is especially due to its osteoconductive and osteoinductive qualities, as well as its immunologic harmlessness14,22,23, whereby the most favorable biological characteristics are ascribed to the cancellous bone.15,16,24 Nonetheless, transplants harvested locally from the mandible or maxillary tuber region do not provide enough bone material for a complete bilateral sinus floor elevation, requiring about 10-15 ml of graft volume.25,26 For this reason, in most cases of extensive augmentations, bone from the iliac crest or proximal tibia, which both provide a sufficiently large bone stock, is used.15,27 However, the proximal tibia has the disadvantage that the cortical portion of the transplant is limited to only the access 7

window27, so that if onlay bone grafting is necessary in addition to the sinus lifting procedure, the iliac crest as a donor site is indispensable.28 Regarding the favorable time for implant insertion, exact information about the three-dimensional resorption of iliac crest grafts, such as are used in sinus floor elevation, would be very helpful, but there is lack of sufficient investigations on this matter thus far.6,29-31 Furthermore, the resorption must be taken into consideration for treatment planning in order to find a sufficient bone volume during the subsequent implantation. The aim of the present clinical study was therefore to quantify the graft’s volume loss after sinus lift surgery with autogenous iliac bone and further to specify the temporal course of transplant resorption. MATERIALS AND METHODS A total of 20 patients -12 female and 8 male- with their age ranging from 34-67 years (a mean 55.2 years) were initially included in the study. All suffered at least unilaterally from an advanced maxillary ridge atrophy with residual crest heights of, on average, 2.7 mm (range: 0.4- 4.2 mm), which did not allow primary implantation. For this reason, in all study participants, a unilateral or bilateral sinus lift was initially performed, in 14 cases combined with an additional onlay bone grafting. Two of our 20 patients received tibial bone within the augmentation; another patient received autogenous bone mixed with a xenogenic graft material (BioOss ®, Geistlich, Switzerland). In all remaining 17 patients, sinus augmentation surgery was carried out utilizing autogenous iliac bone exclusively, in 14 of these bilaterally. Since only these cases of bilateral sinus floor elevation with autogenous iliac grafts and a complete follow-up were incorporated in the final analysis, but three of the 14 patients did not participate in at least one of the follow-up CBCTs, final data processing was confined to a total of 11 patients.

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These 11 patients, including 6 women and 5 men with an average age of 52.3 years, were all non-smokers and showed an inconspicuous general anamnesis at the time of surgery. Preoperatively, they revealed neither clinical nor radiological signs of maxillary sinusitis and, intra-operatively, sinus mucosa presented itself free of inflammation in all cases. According to the routine follow-up of our clinic, all patients underwent cone beam CT (CBCT, GALILEOS Comfort, Sirona, Bensheim, Germany, slice thickness 0.15 mm) of the maxilla immediately after surgery (T0), as well as three (T1) and six (T2) months postoperatively. Surgical procedure All operations were performed under general anesthesia. The surgical technique for the sinus floor elevations followed Tatum's classical description with a bone window prepared in the lateral antral wall, which was created piezosurgically in all cases.8 Simultaneously with the exposure of the upper jaw, a second surgical team gathered a monocorticocancellous bone graft from the anterior iliac crest in the typical manner with preservation of the outer cortical layer. The maximum possible amount of cancellous bone was then collected using Volkmann's spoons of suitable size from the opened marrow spaces. In eight cases, in which advanced maxillary atrophy necessitated an additional onlay bone grafting, bone blocks were shaped from the harvested corticocancellous graft according to the buccal and/ or crestal contour of the alveolar ridge. Subsequent to sinus lifting they were fixed at the maxilla by microscrews and, where necessary, by microplates. The remaining portions of the block graft, and in the cases without onlay grafting, the entire bone blocks were then particulated with the aid of a Tessier bone mill (Stryker-Leibinger, Freiburg, Germany) and, together with the uncrushed spongy bone, they were inserted into the newly created space

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between the bony sinus floor and the Schneiderian membrane. Meticulous care was taken to provide sufficient condensation and an even distribution of the graft material (Figure 1). All patients were treated under stationary conditions and received clindamycin intravenously at a dosage of 600 mg after the induction of anesthesia, and three times daily for five to seven days postoperatively as antibiotic prophylaxis. During the stay in the hospital, with an average duration of 6.3 days (range: 4-10 days), nutrition was provided via a thin nasogastral feeding tube. From discharge until suture removal on day ten postoperatively, a strictly liquid diet was recommended. The gradual pain-dependent mobilization began on the third postoperative day, and from the evening before surgery until discharge, a weight-adapted thrombosis prophylaxis was given subcutaneously with a low molecular weight heparin. Patients were not allowed to blow their nose and advised to administer decongesting nose drops (xylometazoline 0.1%) five to six times per day in both nasal cavities over a period of two weeks. They were also instructed not to wear their maxillary prosthesis for at least 14 days. The healing phase of the bone graft until implant placement lasted at least 5.9 months, with an average of 6.4 months and a maximum of 7.2 months. In total, 59 implants (respectively Camlog Screw-LineTM, Altatec GmbH, Wimsheim, Germany) were inserted into the augmented sinuses. Determination of the graft volumes After importing the DICOM data sets acquired by CBCT scan into the commercially available planning and navigation software iPlan CMF 3.0 (BrainLAB, Feldkirchen, Germany), the bone grafts located on the sinus floor were segmented based on all available standard section planes (axial, coronal, sagittal). For this purpose, a drawing tool is available in iPlan by which the target object can be exactly outlined in each section plane using a mouse cursor. Additionally, the program also permits a gray-scale-based interpolation of up to 8 layers 10

which facilitates the segmentation process and makes it more precise (Figure 2). From these data the software automatically calculates a three-dimensional image of the segmented object, which directly appears in the plan content of iPlan, as well as the object volume (Figure 3). All measurements were conducted by two experienced examiners who first undertook a rehearsal round until the definite volumetric determinations were performed. Subsequently, the mean value of both examiners was calculated and entered the final analysis. Statistical Analysis In addition to descriptive data analysis, a linear mixed model was adapted to the data, with the model building grouping factors such as sex and age (continuous) and the within-subject factors side (right or left) and time (0, 3 and 6 months). Initially we included all two way interaction terms and varied the covariance structure of the within-subject factors. Furthermore, we inspected the distribution of the residuals and checked for influencing observations. Thus it was noticed that the data of patient no. six exerted a high influence on the parameter and covariance parameter estimates. The best fitting model resulted from a model with main effects only. Effects were considered to be significant if the p-values did not exceed the 5 % level. Statistical computations were performed using proc mixed from the Statistical Analysis System software (SAS, 9.1, TS1M3) and the Statistical Package for Social Sciences (SPSS), version 14, under Windows XP. This study was approved by the Aachen University Hospital IRB and all participants signed an informed consent agreement. RESULTS Clinical observations In none of the observed patients postoperative complications such as wound infection, infection of the transplant, major bleeding or persisting swelling occurred. In all cases proper 11

healing of both oral and iliac wounds could be ascertained. Although intraoperatively, a small perforation of the Schneiderian membrane, closed primarily with absorbable sutures, had arisen in one sinus, neither clinical nor radiological signs of a maxillary sinusitis were noted in the postsurgical course. None of the study participants experienced residual complaints like sensory disturbances of the lateral femoral cutaneous nerve or persisting gait problems. At the time of implantation, after an average of 5.4 months, all patients had fully recovered. Volume measurements At the time T0, the average graft volume of the 22 maxillary sinuses, measured in the eleven patients who were considered in the final analysis, amounted to 4.2 cm3. Up to the time T1, significant resorption (p = 0.0001) of 38.9% occurred to a mean bone volume of 2.6 cm3. During the period from T1 to T2, graft volume again decreased significantly (p = 0.0002) by 18.9% (in terms of the initial volume) to a total of 1.8 cm 3, so that at the time of T2 on average 57.8% of the originally transplanted bone was resorbed (Figure 4, Table 1). Within the observed age interval there was no age-specific dependency (p = 0.8813) (Figure 5). Likewise, side specificity could be statistically ruled out (p = 0.078). Furthermore, gender does not exert any consistent effect on the resorption process (p = 0.4367) (Figure 6). Already at T1, all grafts were integrated to host bone on the CBCT scans (Figure 7). DISCUSSION As far as sinus floor elevation surgery is concerned, autogenous bone grafts are still considered favorable.9,17,25,27,32 If there is a marked bony deficit as in the severely atrophied edentulous maxilla, it is inevitable in most cases to draw on extraoral bone donor sites.16,33 The best studied and most widely used extraoral donor site for autogenous bone grafts is undoubtedly the iliac crest.7,16,27,34 Amounts of 7 to 40 ml can be obtained from this site.23,35 Nevertheless, one needs to be aware that a second surgical approach with a certain 12

comorbidity and general anesthesia has to be accepted. In fact, local hematoma, sensory disturbances of the lateral femoral cutaneous nerve, hernias and fractures of the pelvis are described as possible complications of graft harvesting from the iliac crest.36 Younger and Chapman (1989)37 indicate a rate of 8.6% of serious complications in the conventional open harvesting technique, which we, however, consider to be too high according to our own clinical experience. To reduce the possible complications, Caminiti et al. (1999)38 recommended the open removal of bone cylinders with suitable trephine drills by which, however, only small amounts of bone between 2.3 to 3.2 ml can be gathered. Also, intraoral donor sites such as the ascending mandibular ramus and the chin region provide a maximum volume of cortical and cancellous bone of only 2 to 5 ml25,26 - enough to fill up small defects such as extraction wounds or periodontal lesions, but too low for extensive augmentations. For a complete bilateral sinus lift, for example, a bone amount of 10 to 15 ml is required.25,26 In the study in hand, a bone quantity of an average 4.2 ml per sinus was transplanted. Here it should be noted that this is a kind of net volume of the inserted bone after condensation. In 8 patients an additional onlay osteoplasty was performed, which made an open removal of pelvic bone unavoidable. Over the course of our investigation, the tremendous volume loss of the transplanted bone became very clear. To be precise, within 6 months 57.8% of the graft was resorbed. This rather high bone loss exceeds the values of 21-51% stated in the literature, which nevertheless are in no case based on three-dimensional measurements.21,34,39-41 Basically, the removal technique or the handling of the bone graft, as well as the method of augmentation could entail major sources of error. Yet, in all surgeries performed within this study, meticulous care was taken to provide gentle treatment as well as an optimum preparation of the bone graft. Indeed, the removed cancellous bone was not further particulated to preserve the osteoblasts and precursor cells; however, the cortical bone block was minced in a bone mill to increase the surface of osteoinductive and osteoconductive material.42 Admittedly, particulated bone 13

grafts are considered to exhibit more intense sintering than block transplants associated with a resorption rate of up to 20 %.21,44 In order to minimize this effect, great importance was extended to equal distribution and sufficient compaction of the graft material. During the preparation of the recipient bed at the maxillary sinus floor, only one case of mucosa perforation occurred. This could be primarily closed with absorbable sutures. To overcome the high failure rate of implants in connection with transplanted bone during single-stage surgery, the implant placement was carried out in two stages, respectively.22,39 However, what further factors could be responsible for the observed distinctly high resorption rate? Certainly, lack of physiological load of the grafted bone is one major problem in terms of volume stability. Accordingly, Sbordone and coworkers report on negligible resorption rates of less than 7 % one year after implant insertion into sinuses elevated by particulated crest grafts.40 There is also evidence that microbial contamination might be associated with an increased loss of bone volume subsequent to sinus lifting surgery with autogenous bone.41 Finally, the method of volume measurements could be sensitive to analysis bias; however, all definite measurements were performed by two experienced examiners after undertaking a rehearsal round, and there was a difference of less than 13 % between both volume determinations. Because of this, and the small sample size, we abstained from calculating the kappa value to determine inter-examiner variability. In this context it should also be emphasized that the grey-scale values of the utilized CBCT were not based on Hounsfield units, which is why we refrained from bone density measurements; this, of course, is a weakness of the investigation in hand that the chosen method does not allow a statement on the density of the remodeled bone graft compared to the host bone. The findings of the current study stand in sharp contrast to the volume stability of bone substitute materials which, according to Gassmann & Dawirs (2010)20, can be successfully applied as a replacement of autogenous bone grafts. Despite the high success rate of bone substitute materials, such defect morphologies requiring block grafts can so far be treated best 14

with the aid of autologous bone containing all components such as osteoblasts, osteoprogenitor cells, as well as growth factors and cytokines that are necessary for a successful replacement of larger jaw sections.32 Over and above that, the absence of biologically important osteoblastic cells delays the healing of alloplastic bone substitutes, and, with the exception of a significantly prolonged resorption, inflammatory responses can occasionally be observed.13,20,27 Accordingly, it would be ideal to find a way to take advantage of the favorable properties of autogenous grafts, but to circumvent their enormous resorption. For this purpose, various possibilities are conceivable: Firstly, bone substitute materials can be added to autogenous grafts in terms of protection against resorption as acid-resistant bone substitutes such as BioOss ® (Geistlich, Switzerland) represent a barrier for the degradation of osteoblasts caused by acids.43,44 Ideally, the bone substitute material would have to be located on the periphery of the bone graft. Secondly, the lateral access window can be covered by a membrane to inhibit the access of osteoclasts and to thus create a barrier for resorption.19,20,44,45 On the other hand, the interruption of periosteal blood supply prevents nutrients, BMPs and osteoprogenitor cells from interacting with the grafted bone material.21 However, it might be much easier and just as effective -as our results undoubtedly indicate – to perform implant placement just three months after sinus floor elevation with autogenous bone because the grafts will already be fully integrated by this time. Thereby the transplanted bone is protected against further resorption by the earlier onset of functional load.40,44,46 Furthermore, former studies have shown that revascularization has taken place within 30 days, and remodeling of the graft is already completed within 90 days.47,48 Indeed, all iliac grafts were radiologically fully integrated into the maxillary bone at T1 after 3 months. Therefore the healing time is much shorter than with alloplastic materials. For the patient, the earlier implant placement includes the tremendous advantage of being able to wear a functional denture at a much earlier stage.49 However, the surgeon is obliged to discuss 15

different treatment options with each individual patient discussing risks and benefits of autogenous bone grafting versus the use of biomaterials on an individual basis. 50, 51

CONCLUSIONS In conclusion, it can be stated that in sinus floor elevation autogenous iliac bone grafts are characterized by a high resorption rate, at least as long as they are not functionally loaded. Therefore, a healing time of six months until implant insertion is definitely too long. Surgical strategies must be considered to reduce resorption of the graft volume observed when using iliac autogenous bone.

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1. Atwood D. Bone loss of edentulous alveolar ridges. J Periodontol. 1979; 50: 11-21. 2. Smiler DG, Johnson PW, Lozada JL, Misch C, Rosenlicht JL, Tatum OH Jr, Wagner JR. Sinus lift grafts and endosseous implants. Treatment of the atrophic posterior maxilla. Dent Clin North Am. 1992; 36: 151-186. 3. van den Bergh JP, ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus floor elevations. Clin Oral Implants Res. 2000; 11: 256-265. 4.

Garg AK. Augmentation grafting of the maxillary sinus for placement of dental implants: anatomy, physiology, and procedures. Implant Dent. 1999; 8: 36-46.

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FIGURE CAPTIONS Fig. 1

Condensed and distributed graft material on the maxillary sinus floor

Fig. 2

Gray-scale based interpolation of 8 layers in iPlan CMF 3.0 (BrainLAB, Feldkirchen, Germany)

Fig. 3

A three dimensional picture of the segmented bone graft and its volume appear in the plan content

Fig. 4

Bone volume in cm3 (y-axis) at the time of T0, T1 and T2 (x-axis): a significant resorption of 57.8% between T0 and T2 can be seen

Fig. 5

Pearson’s correlation of age and bone loss between T0 and T2: no age-specific dependency can be observed

Fig. 6

Effect of gender on bone graft’s resorption: no significant effect on the resorption process can be seen

Fig. 7

Bone graft at the time of T1: the transplant presents itself fully osseously integrated

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Figure 1 Click here to download high resolution image

Figure 2 Click here to download high resolution image

Figure 3 Click here to download high resolution image

Figure 4 Click here to download high resolution image

Figure 5 Click here to download high resolution image

Figure 6 Click here to download high resolution image

Figure 7 Click here to download high resolution image

Table Click here to download Table: Table 1.docx

TABLE 1 Overview on the results differentiated with regard to sex, time and grafted side Graft Volume CBCT N Mean

SD

Min

Median

Max

SEX

MONTH

SIDE

m

0

1

5 5.340 1.591 3.091

6.263

6.784

2

5 5.326 1.969 2.103

6.269

6.829

1

5 3.409 0.881 2.224

3.347

4.589

2

5 3.507 1.659 1.244

4.179

5.185

1

5 2.287 1.036 1.106

2.246

3.366

2

5 2.563 1.555 0.524

2.821

4.055

1

6 3.712 2.266 1.562

2.605

6.720

2

6 3.216 1.840 0.908

3.113

6.125

1

6 2.295 1.378 1.276

1.903

4.833

2

6 1.934 0.959 0.838

1.639

3.432

1

6 1.695 1.481 0.682

1.268

4.624

2

6 1.301 0.601 0.426

1.362

1.921

3

6

f

0

3

6

21

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