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Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest
Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
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Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest T. Fretwurst a, *, C. Nack b, M. Al-Ghrairi b, J.D. Raguse b, A. Stricker a, R. Schmelzeisen a, K. Nelson a, S. Nahles b a
Department of Oral and Craniomaxillofacial Surgery, Center for Dental Medicine, University Medical Center Freiburg, Hugstetter Straße 55, D-79106 Freiburg, Germany Department of Oral and Maxillofacial Surgery, Navigation and Robotics, Charit e Campus Virchow, Berlin, Germany
b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 30 November 2014 Accepted 27 March 2015 Available online xxx
Objective: The purpose of the present study was to evaluate crestal bone level changes around dental implants after iliac bone augmentation in the long term. Material and methods: A total of 32 partially edentulous/edentulous patients (mean age, 52 years; range, 22e70 years) and a remaining bone volume of less than 5 mm of the alveolar ridge underwent maxillary or mandibular iliac bone graft augmentation. All patients received spaced standardized radiological examination for evaluation of peri-implant crestal bone loss. Results: The grafting procedure was successfully performed in all patients. A total of 150 implants were placed. The mean observation period was 69 months (range, 12e165 months; success rate for maxilla, 96%; success rate for mandible, 92%). The mean amount of crestal bone loss after 10 years was 1.8 mm. A significant difference between gender and crestal bone loss was shown, but no influence was found regarding the implant system, diameter of implant, and age of the patients. Conclusion: In patients with atrophic jaws, a sufficient long-term reconstruction can be achieved with the combination of iliac onlay grafting and dental implants. The results demonstrate high success rates and a stable peri-implant bone level in the long term. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Augmentation Crestal bone level Long-term Autogenous Bone resorption Extreme atrophy
1. Introduction The restoration of the oral function of extremely atrophied alveolar crests remains a task in oral and maxillofacial surgery. Severe atrophy of maxilla and mandible can be treated successfully with various augmentation procedures in combination with dental implant systems (Vermeeren et al., 1996; Reinert et al., 2003; Whitmyer et al.; 2003; Nelson et al., 2006a,b). In patients with minimal residual bone, autogenous bone from the iliac crest remains the gold standard, providing the properties necessary for bone remodeling: osteoinduction, osteoconduction,
* Corresponding author. Department für Zahn-, Mund- und Kieferheilkunde, Klinik für Mund-, Kiefer- und Gesichtschirurgie/Plastische Operationen, Uni€tsklinikum Freiburg, Albert Ludwig Universit€ versita at Freiburg, Hugstetter Str. 55, D-79106 Freiburg, Germany. Tel.: þ49 761 270 47010; fax: þ49 761 270 48770. E-mail address: [email protected] (T. Fretwurst).
and osteogenic potential (Lundgren et al., 1999; van der Meij et al., 2005; Chiapasco et al., 2007; Moses et al., 2007; Sbordone et al.; 2014). The authors showed an implant survival rate up to 98.7% within a 5-year period after iliac crest onlay grafting in the mandible (Boven et al., 2014). However, a vertical unpredictable bone loss with a severe discrepancy between the resorption rates is described in literature and may compromise the long-term survival of the placed implants (Adell et al., 1990; € m et al., 1996; Verhoeven et al., 2000, 2006; Bell et al., Nystro 2002; Verhoeven et al., 2006; Dasmah et al., 2012; Boven et al., 2014). van der Meij reported an average resorption of 15% of the initial graft after a follow-up to 7.9 years (van der Meij et al., 2005). In a 5-year follow-up after corticocancellous augmentation, an overall bone resorption rate of up to 50% has been described (Vermeeren et al., 1996; Verhoeven et al., 2006). Strategies to minimize bone resorption have been proposed (Wiltfang et al., 2014).
http://dx.doi.org/10.1016/j.jcms.2015.03.037 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
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T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
The anterior iliac crest is a common donor site, with the superioreanterior rim of the iliac crest commonly presenting a large € mnez et al., 2013; Zaker cortical segment (Ebraheim et al., 1997; So Shahrak et al., 2014). Other authors prefer a posterior donor site to harvest a large portion of cancellous bone matched with a low complication rate (Wiltfang et al., 2005). Long-term studies concerning dental implants placed in illiac onlay grafts exist, but an evaluation of the peri-implant bone level is rare (Verhoeven et al., 2006; Chiapasco et al., 2008, 2014; Sbordone et al., 2012; Boven et al., 2014). The aim of this study was to evaluate crestal bone level changes around dental implants placed in onlay bone grafts harvested from the anterior superior iliac rim in the long term. 2. Material and methods This study was approved by the local ethical committee of the Medical University Berlin, Germany. Charite 2.1. Study design and sample In the period starting from 1998, 32 patients (22 female and 10 male) with a mean age of 52 years (range, 22e70 years) underwent maxillary or mandibular onlay augmentation with iliac bone grafts and were re-examined in 2012. All patients were partially edentulous or edentulous and showed a severe resorption of the alveolar ridge with a remaining bone volume of 5 mm in height. In all of the patients, onlay grafting with corticocancellous bone from the anterior superior iliac crest was performed. The anterior ilium has a concave anterosuperior surface and presents a thick cortical rim (iliac tubercle) 2e3 cm posterior to the anterior superior iliac spine. In this study, corticocancellous bone blocks with a cortical rim of 4 mm were harvested from the median margin of the anterior iliac crest. 2.2. Exclusion criteria Age less than 18 years, periodontitis, history of immunosuppression, irradiation, or chemotherapy, and participation in other studies were exclusion criteria.
Fig. 1. Harvested corticocancellous iliac graft with two curved cortical walls and a cancellous internal part.
grafting procedures were performed according to a standard protocol. The patients were given an intravenous antibiotic regimen (clindamycin 600 mg) during the operation and oral antibiotics postoperatively (clindamycin 300 mg three times a day) for 7 days. All patients remained hospitalized for 2e3 days. The iliac sutures were removed after 10 days. All patients were clinically evaluated after 1, 3, 10, and 30 days as well as after 3 and 6 months. The clinical evaluation included assessment of complications such as inflammation, mucosal erythema, wound dehiscences, and loss of bone grafts. Standardized radiographic examinations (orthopantomograms) were performed before and immediately after the surgical procedure, after 1, 3, 5, and 10 years. 2.4. Implant placement
2.3. Surgical procedure Surgery for bone augmentation and implant placement was performed under general anesthesia. The harvesting of the iliac graft was performed as described (Fretwurst et al., submitted for publication). After removal of the corticocancellous bone block from the inner table, additional cancellous bone was harvested with curettes. Ideally the harvested bone has a curved cortical wall and a cancellous internal part (Fig. 1). The size and contour of onlay grafts were limited to the size needed for an appropriate implant length (height, 9e16 mm). Intraorally, a slightly palatal crestal incision along the edentulous alveolar crest with distal and median vertical releasing incisions was performed, and a mucoperiosteal flap was raised. In cases with a combination of onlay graft and sinus elevation procedures, a standard sinus floor elevation was performed with cancellous bone (Boyne and James, 1980). The corticocancellous bone blocks were contoured and fixed to the labial and occlusal aspect of the alveolar ridge, so that the cortical wall faces occlusal and vestibular. Each bone block was secured with multiple microscrews (Modus 1.5; Medartis, Umkirch, Germany). The mucoperiosteal flap was passively mobilized and closed with a running suture and secured with four to five interrupted sutures (5-0 Monocryl; Ethicon, Norderstedt, Germany). All bone
After a healing period of 3 months, the previous incision line used in the grafting procedure was used for the preparation of a mucoperiosteal flap to remove the microscrews and to place the dental implants. Among all 32 patients, a total of 150 implants were placed according to the manufacturer's surgical protocol; 99 were Camlog RootLine implants (Camlog Biotechnologies, Wimsheim, Germany), 28 were Straumann Tissue Level implants (Straumann AG, Basel, Switzerland), and 23 were Steri-Oss implants (Nobel Biocare Deutschland GmbH, Cologne, Germany). The Camlog and Steri-Oss implants were inserted equicrestally. All Straumann implants were placed with the smootherough border at the crestal bone level. The mucoperiosteal flaps were closed with a running suture and secured with random interrupted sutures (5-0 Monocryl, Ethicon, Norderstedt, Germany). The time of unloaded healing of the implants was 12 weeks for maxillary implants and 8 weeks for mandibular implants. At loading, the stability of the implant was reassessed using a torque ratchet. If the torque value of the implant was >35 Ncm, then the prosthetic treatment was initialized. All patients received splinted prosthetic treatment. The patients were either restored with removable dentures seated on individually fabricated bars or with fixed bridges.
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
2.5. Radiographic evaluation All patients received spaced standardized radiological examination for evaluation of peri-implant crestal bone loss. The quantitative evaluation of the crestal bone loss was analyzed on routinely taken orthopantomographs as described previously mez-Roman et al., 1997; Semper et al., 2010; Heberer et al., (Go 2011; Nack et al., 2014). Conventional radiographs (Orthophos Plus, Sirona, Bensheim, Germany) were not digitized and were analyzed using a previously published method (Semper et al., 2010; Heberer et al., 2011). Digital orthopantomographs (Orthophos XG 5/Ceph, Sirona, Bensheim, Germany) were analyzed with Kodak Dental Imaging Software 6.8 (Carestream Dental, Stuttgart, Germany). The measurements of the vertical changes in the marginal bone were performed at described time points t0 (postoperatively ¼ baseline), t1 (after 1 year), t2 (after 3 years), t3 (after 5 years), and t4 (after 10 years) five times at the mesial (m) and distal (d) sites of the implant. To eliminate radiographic distortions, the values were adjusted with respect to the original length of the implant. The interpretation of the values of the mesial and distal sites was performed separately, and the mean values for all sites (mesial/ distal) were determined as follows: m1/d1 ¼ value of mesial/distal bone contact from the reference point after 1 year; m2/d2 ¼ value of mesial/distal bone contact from the reference point after 3 years; m3/d3 ¼ value of mesial/distal bone contact from the reference point after 5 years; and m4/d4 ¼ value of mesial/distal bone contact from the reference point after 10 years. Bone level changes were analyzed by subtracting the values of bone loss from the initial postoperative value. 2.6. Statistical analysis The intraclass correlation coefficient (ICC) was used to determine the intraobserver reliability using SPSS 16.0 software (SPSS Inc., Chicago, IL, USA). Besides the descriptive evaluation of the data, the correlations between diameter, age, gender, and localization with mesial and distal bone level changes were analyzed using the ManneWhitney U-test and the Spearman rank-order correlation coefficient. The mesial and distal sites were analyzed separately. Statistical analyses were performed using the SPSS 13.0 software (SPSS Inc.) and SAS, Version 9.1 (SAS Institute Inc., Cary, NC, USA). A p-value of <0.05 was considered statistically significant.
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Table 1 Data for crestal bone loss at all implants over an observation period of up to 120 months. Bone level (mm) t1 Maxillary Mandible Mesial Distal
0.9 1.0 0.8 0.9
t2 (0e3.5) (0e2.2) (0e3) (0e4)
1.4 1.1 1.4 1.4
t3 (0.1e3.8) (0.2e2.7) (0e4) (0.1e4)
1.7 1.8 1.8 1.7
t4 (0.1e4.0) (0.5e2.9) (0e4) (0.2e4)
1.8 (0.4e4.0) 1.8 (0.5e4) 1.8 (0.5e4)
Baseline: t1, 1 year; t2, 3 years; t3, 5 years; t4, 10 years. Table 2 Data for crestal bone loss at all implants over an observation period of more than 60 months. Bone level (mm)
Mesial Distal
t1
t2
t3
t4
0.9 0.8
1.4 1.4
1.8 1.7
1.8 1.8
Baseline: t1, 1 year; t2, 3 years; t3, 5 years; t4, 10 years.
0.5e4 mm) and in male patients a mean bone level change of 1 mm (range, 0.5e2 mm) were documented after 10 years. Of all implants, 92 had a follow-up of 5 or more years; mean values of bone level changes of this observation period are listed in Table 2. Statistical analysis showed that there was a significant difference between genders (Pmesialþdistal<0.01) regarding the crestal bone loss after 10 years, but no significant difference was found between the diameter of the implants (Pmesial ¼ 0.26, Pdistal ¼ 0.68), implant systems (Pmesial ¼ 0.37, Pdistal ¼ 0.15), and age (Pmesial ¼ 0.13, Pdistal ¼ 0.68) (Fig. 2). Length, diameter, frequency, and manufacturer of the implant systems used are shown in Table 3. 4. Discussion The present study demonstrates that patients with atrophied jaws can undergo sufficient reconstruction with current dental
3. Results A total of 150 implants were placed (23 Steri-Oss, 99 Camlog and 28 Straumann). The mean observation period of all implants was 69 months (range, 12e165 months). A total of 88 implants (maxilla, 83, mandible, 5) were followed up for more than 5 years, and 29 implants were followed up for an observation period of 13 years. The mean observation period of the maxilla with 125 implants (23 Steri-Oss, 82 Camlog implants, 20 Straumann) was 75 months (range, 12e165 months) and of the mandible with 25 implants (17 Camlog implants, 8 Straumann implants); the mean follow-up was 42 months (range, 12e91 months). During the observation period, seven implants (5 maxillary and 2 mandibular implants) were lost. Two implants in the lower jaw were lost prior to loading due to a failed osseointegration. No second implant insertion was performed. One implant was lost in the maxilla after 6 years and four maxillary implants after 8 years due to peri-implantitis. The survival rate of the implants was 95% (maxilla, 96%; mandible, 92%). The mean values of bone level changes over time are listed in Table 1. In female patients a mean crestal bone loss of 2 mm (range,
Fig. 2. Box-plot showing the significant difference of the crestal bone loss between the gender after ten years (M-Male, F-Female, mesialemesial implant site, distaledistal implant site).
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
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T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
Table 3 Lengths, diameters, frequencies, and manufacturers of the implant systems used. System
Diameter
Frequency
%
Steri-Oss
3,3 3,8 4,5 Total 3,8 4,3 5,0 6,0 Total 3,3 4,1 Total
4 14 5 23 63 33 2 1 99 2 26 28
17.4 60.9 21.7 100.0 63.4 33.3 2.0 1.0 100.0 7.1 92.9 100.0
Camlog
Straumann
System
Length
Frequency
%
Steri-Oss
10 12 14 16 Total 9 11 13 16 Total 10 12 Total
1 14 4 4 23 4 45 45 5 99 17 11 28
4.3 60.9 17.4 17.4 100.0 4.0 45.5 45.5 5.0 100.0 60.7 39.3 100.0
Camlog
Straumann
implant systems after iliac onlay bone grafting with an overall implant survival rate of 95% in the long term. The longest observation period was 13 years. The present implant survival rates are comparable with other long-term follow-up studies. The implant survival rates were 98.7% after 5.5 years, 100% up to 6 years, 96.7% after 9 years, and 100% after 10 years (patient collective range, 13e40) (Verhoeven et al., 2006; Chiapasco et al., 2008; Sbordone et al., 2012; Boven et al., 2014). In the 1970s, iliac crest augmentation was used only to improve prosthetic rehabilitation without implant insertion, resulting in an almost complete resorption of the autogenous graft (Curtis et al., 1977). The one-step technique (bone augmentation with immediate implant insertion) showed problems comprising insufficient implant positioning for prosthetic rehabilitation and tissue dehiscence (Nystrom et al., 1993). At the end of the 1990s, the two-stage method was established, with a 6-month healing period for the iliac graft (Lundgren et al., 1997). Since then, the timing of implant placement, whether simultaneous or delayed, has been discussed € stro €m et al., in the literature extensively (Lundgren et al., 1997; Sjo 2006; Verhoeven et al., 2006). There are a few long-term studies after iliac crest grafting evaluating the peri-implant bone level €stro € m et al. 2007; changes with a graft healing time of 6 months (Sjo €m et al., 2009). Other studies showed that 3 months of Nystro healing both for the graft and the implants is sufficient for the revascularization of the graft and the secure insertion of roughsurfaced dental implants as well as the loading of the implants (Nelson et al., 2006a,b; Heberer et al., 2009; Semper et al., 2010). In this study, the two-step technique with an implant insertion after 3 months was applied because several authors reported better implant integration and positioning with this approach (Lundgren € stro €m et al., 2006). The success rates in this study et al., 1997; Sjo justify this concept and healing period. In the present study, the major crestal bone loss appears within the first year. On average, less than 1 mm is lost in the first year. This is observed in implants placed in avascular fibula grafts and in nonaugmented regions as well. The results within this study demonstrate that the implants placed in augmented bone revealed
similar bone level changes compared to implants inserted in nonaugmented regions (Jemt et al., 1996; Nelson et al., 2006a,b; Semper et al., 2010). Several authors of comparable studies did not measure the periimplant bone level after implant insertion (Verhoeven et al., 2006; Sbordone et al., 2012). Data from Boven et al. are difficult to compare, as only an accumulated mean radiographic marginal bone loss (0.6 ± 0.7 mm) is shown at least after 5 years (Boven et al., 2014). Chiapasco et al. confirm the present data; there is also approximately 1 mm peri-implant bone loss detected after 1 year. After 5 years, still 1 mm is lost. However, the aforementioned study is limited: Only the lower jaw was examined, and in the period between loading and recall after 10 years, the number of implants was halved (Chiapasco et al., 2008). Strategies to minimize bone resorption after autogenous grafting are discussed in the literature (Cordaro et al., 2011; Wiltfang et al., 2014). The additional application of deproteinized bovine bone matrix (DBBM) has been shown to reduce bone resorption of autogenous grafts (Maiorana et al., 2005; Wiltfang et al., 2005; Maestre-Ferrin et al., 2009; Cordaro et al., 2011; Wiltfang et al., 2014). A cohort study with similar defect sizes, age, and gender distribution showed that DBBM coverage of the iliac crest graft reduced the early bone resorption (12 months) postoperatively, but long-term data are missing (Wiltfang et al., 2014). The age of the patient or implant system used had no impact on the survival rate or crestal bone loss, whereas gender seemed to be of importance. Females showed significantly more marginal bone loss than males after 10 years. This might be due to a difference in individual factors influencing bone physiology. Estrogens and androgens are discussed in bone health and preservation (Manolagas et al., 2013). The sex steroid hormones maintain a balance between bone formation and resorption through changes in osteoclastogenesis and osteoblastogenesis (Manolagas et al., 2013). The interindividual, gender-specific hormone status may play a role in bone physiology of oral autologous grafts. However, further studies are necessary to identify factors influencing bone resorption. In previous studies, often only survival rates were documented as parameters of success; however, peri-implant bone loss rates should be considered as well. 5. Conclusion The reconstruction of atrophic jaws with cortico-cancellous bone grafts from the anterior superior iliac crest and placement of endosseous implants is a predictable technique to facilitate longterm rehabilitation of the extremely atrophic jaw. The mean periimplant bone loss is comparable to that found in nonaugmented bone. The overall implant survival rate exceeds 95%. Conflict of interest The authors reported no conflicts of interest related to this study. Acknowledgment This study was partially funded by the Camlog Foundation (CF41306). References €ndahl K, Brånemark PI, Lindstro € m J, Jacobsson M: ReconAdell R, Lekholm U, Gro struction of severely resorbed edentulous maxillae using osseointegrated fixtures in immediate autogenous bone grafts. Int J Oral Maxillofac Implants 5(3): 233e246, 1990
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Nelson K, Ozyuvaci H, Bilgic B, Klein M, Hildebrand D: Histomorphometric evaluation and clinical assessment of endosseous implants in iliac bone grafts with shortened healing periods. Int J Oral Maxillofac Implants 21(3): 392e398, 2006a Nelson K, Glatzer C, Hildebrand D, Hell B, Klein M: Clinical evaluation of endosseous implants in nonvascularized fibula bone grafts for reconstruction of the severely atrophied mandibular bone. J Oral Maxillofac Surg 64(9): 1427e1432, 2006b Nystrom E, Kahnberg KE, Gunne J: Bone grafts and Brånemark implants in the treatment of the severely resorbed maxilla: a 2-year longitudinal study. Int J Oral Maxillofac Implants 8(1): 45e53, 1993 €m E, Ahlqvist J, Kahnberg KE, Rosenquist JB: Autogenous onlay bone grafts Nystro fixed with screw implants for the treatment of severely resorbed maxillae. Radiographic evaluation of preoperative bone dimensions, postoperative bone loss, and changes in soft-tissue profile. Int J Oral Maxillofac Surg 25: 351e359, 1996 €m E, Nilson H, Gunne J, Lundgren SA: 9-14 year follow-up of onlay bone Nystro grafting in the atrophic maxilla. Int J Oral Maxillofac Surg 38(2): 111e116, 2009 €nig S, Bremerich A, Eufinger H, Krimmel M: Stability of bone grafting Reinert S, Ko and placement of implants in the severely atrophic maxilla. Br J Oral Maxillofac Surg 41(4): 249e255, 2003 Sbordone C, Toti P, Guidetti F, Califano L, Santoro A, Sbordone L: Volume changes of iliac crest autogenous bone grafts after vertical and horizontal alveolar ridge augmentation of atrophic maxillas and mandibles: a 6-year computerized tomographic follow-up. J Oral Maxillofac Surg 70(11): 2559e2565, 2012 Sbordone C, Toti P, Guidetti F, Califano L, Pannone G, Sbordone L: Volumetric changes after sinus augmentation using blocks of autogenous iliac bone or freeze-dried allogeneic bone. A non-randomized study. J Craniomaxillofac Surg 42(2): 113e118, 2014 Semper W, Heberer S, Nelson K: Retrospective analysis of bar-retained dentures with cantilever extension: marginal bone level changes around dental implants over time. Int J Oral Maxillofac Implants 25(2): 385e393, 2010 €stro €m M, Lundgren S, Sennerby L: A histomorphometric comparison of the bone Sjo graft-titanium interface between interpositional and onlay/inlay bone grafting techniques. Int J Oral Maxillofac Implants 21(1): 52e62, 2006 €stro €m M, Sennerby L, Nilson H, Lundgren S: Reconstruction of the atrophic Sjo edentulous maxilla with free iliac crest grafts and implants: a 3-year report of a prospective clinical study. Clin Implant Dent Relat Res 9(1): 46e59, 2007 € nmez TT, Prescher A, Salama A, Kanatas A, Zor F, Mitchell D, et al: Comparative So clinicoanatomical study of ilium and fibula as two commonly used bony donor sites for maxillofacial reconstruction. Br J Oral Maxillofac Surg 51(8): 736e741, 2013 van der Meij EH, Blankestijn J, Berns RM, Bun RJ, Jovanovic A, Onland JM, et al: The combined use of two endosteal implants and iliac crest onlay grafts in the severely atrophic mandible by a modified surgical approach. Int J Oral Maxillofac Surg 34(2): 152e157, 2005 Verhoeven JW, Ruijter J, Cune MS, Terlou M, Zoon M: Onlay grafts in combination with endosseous implants in severe mandibular atrophy: one year results of a prospective, quantitative radiological study. Clin Oral Implants Res 11(6): 583e594, 2000 Verhoeven JW, Cune MS, Ruijter J: Permucosal implants combined with iliac crest onlay grafts used in extreme atrophy of the mandible: long-term results of a prospective study. Clin Oral Implants Res 17(1): 58e66, 2006 Vermeeren JI, Wismeijer D, van Waas MA: One-step reconstruction of the severely resorbed mandible with onlay bone grafts and endosteal implants. A 5-year follow-up. Int J Oral Maxillofac Surg 25(2): 112e115, 1996 Whitmyer C, Esposito SJ, Alperin S: Longitudinal treatment of a severely atrophic mandible: a clinical report. J Prosthet Dent 90(2): 116e120, 2003 Wiltfang J, Schultze-Mosgau S, Nkenke E, Thorwarth M, Neukam FW, Schlegel KA: Onlay augmentation versus sinuslift procedure in the treatment of the severely resorbed maxilla: a 5-year comparative longitudinal study. Int J Oral Maxillofac Surg 34(8): 885e889, 2005 €tschmann N, Hedderich J, Neukam FW, Schlegel KA, Gierloff M: Effect Wiltfang J, Ja of deproteinized bovine bone matrix coverage on the resorption of iliac corticospongeous bone graftsda prospective study of two cohorts. Clin Oral Implants Res 25(2): e127ee132, 2014 Zaker Shahrak A, Zor F, Kanatas A, Acikel C, Sapountzis S, Nicoli F, et al: Morphological and morphometric evaluation of the ilium, fibula, and scapula bones for oral and maxillofacial reconstruction. Microsurgery 34(8): 638e645, 2014
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Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest T. Fretwurst a, *, C. Nack b, M. Al-Ghrairi b, J.D. Raguse b, A. Stricker a, R. Schmelzeisen a, K. Nelson a, S. Nahles b a
Department of Oral and Craniomaxillofacial Surgery, Center for Dental Medicine, University Medical Center Freiburg, Hugstetter Straße 55, D-79106 Freiburg, Germany Department of Oral and Maxillofacial Surgery, Navigation and Robotics, Charit e Campus Virchow, Berlin, Germany
b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 30 November 2014 Accepted 27 March 2015 Available online xxx
Objective: The purpose of the present study was to evaluate crestal bone level changes around dental implants after iliac bone augmentation in the long term. Material and methods: A total of 32 partially edentulous/edentulous patients (mean age, 52 years; range, 22e70 years) and a remaining bone volume of less than 5 mm of the alveolar ridge underwent maxillary or mandibular iliac bone graft augmentation. All patients received spaced standardized radiological examination for evaluation of peri-implant crestal bone loss. Results: The grafting procedure was successfully performed in all patients. A total of 150 implants were placed. The mean observation period was 69 months (range, 12e165 months; success rate for maxilla, 96%; success rate for mandible, 92%). The mean amount of crestal bone loss after 10 years was 1.8 mm. A significant difference between gender and crestal bone loss was shown, but no influence was found regarding the implant system, diameter of implant, and age of the patients. Conclusion: In patients with atrophic jaws, a sufficient long-term reconstruction can be achieved with the combination of iliac onlay grafting and dental implants. The results demonstrate high success rates and a stable peri-implant bone level in the long term. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Augmentation Crestal bone level Long-term Autogenous Bone resorption Extreme atrophy
1. Introduction The restoration of the oral function of extremely atrophied alveolar crests remains a task in oral and maxillofacial surgery. Severe atrophy of maxilla and mandible can be treated successfully with various augmentation procedures in combination with dental implant systems (Vermeeren et al., 1996; Reinert et al., 2003; Whitmyer et al.; 2003; Nelson et al., 2006a,b). In patients with minimal residual bone, autogenous bone from the iliac crest remains the gold standard, providing the properties necessary for bone remodeling: osteoinduction, osteoconduction,
* Corresponding author. Department für Zahn-, Mund- und Kieferheilkunde, Klinik für Mund-, Kiefer- und Gesichtschirurgie/Plastische Operationen, Uni€tsklinikum Freiburg, Albert Ludwig Universit€ versita at Freiburg, Hugstetter Str. 55, D-79106 Freiburg, Germany. Tel.: þ49 761 270 47010; fax: þ49 761 270 48770. E-mail address: [email protected] (T. Fretwurst).
and osteogenic potential (Lundgren et al., 1999; van der Meij et al., 2005; Chiapasco et al., 2007; Moses et al., 2007; Sbordone et al.; 2014). The authors showed an implant survival rate up to 98.7% within a 5-year period after iliac crest onlay grafting in the mandible (Boven et al., 2014). However, a vertical unpredictable bone loss with a severe discrepancy between the resorption rates is described in literature and may compromise the long-term survival of the placed implants (Adell et al., 1990; € m et al., 1996; Verhoeven et al., 2000, 2006; Bell et al., Nystro 2002; Verhoeven et al., 2006; Dasmah et al., 2012; Boven et al., 2014). van der Meij reported an average resorption of 15% of the initial graft after a follow-up to 7.9 years (van der Meij et al., 2005). In a 5-year follow-up after corticocancellous augmentation, an overall bone resorption rate of up to 50% has been described (Vermeeren et al., 1996; Verhoeven et al., 2006). Strategies to minimize bone resorption have been proposed (Wiltfang et al., 2014).
http://dx.doi.org/10.1016/j.jcms.2015.03.037 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
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T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
The anterior iliac crest is a common donor site, with the superioreanterior rim of the iliac crest commonly presenting a large € mnez et al., 2013; Zaker cortical segment (Ebraheim et al., 1997; So Shahrak et al., 2014). Other authors prefer a posterior donor site to harvest a large portion of cancellous bone matched with a low complication rate (Wiltfang et al., 2005). Long-term studies concerning dental implants placed in illiac onlay grafts exist, but an evaluation of the peri-implant bone level is rare (Verhoeven et al., 2006; Chiapasco et al., 2008, 2014; Sbordone et al., 2012; Boven et al., 2014). The aim of this study was to evaluate crestal bone level changes around dental implants placed in onlay bone grafts harvested from the anterior superior iliac rim in the long term. 2. Material and methods This study was approved by the local ethical committee of the Medical University Berlin, Germany. Charite 2.1. Study design and sample In the period starting from 1998, 32 patients (22 female and 10 male) with a mean age of 52 years (range, 22e70 years) underwent maxillary or mandibular onlay augmentation with iliac bone grafts and were re-examined in 2012. All patients were partially edentulous or edentulous and showed a severe resorption of the alveolar ridge with a remaining bone volume of 5 mm in height. In all of the patients, onlay grafting with corticocancellous bone from the anterior superior iliac crest was performed. The anterior ilium has a concave anterosuperior surface and presents a thick cortical rim (iliac tubercle) 2e3 cm posterior to the anterior superior iliac spine. In this study, corticocancellous bone blocks with a cortical rim of 4 mm were harvested from the median margin of the anterior iliac crest. 2.2. Exclusion criteria Age less than 18 years, periodontitis, history of immunosuppression, irradiation, or chemotherapy, and participation in other studies were exclusion criteria.
Fig. 1. Harvested corticocancellous iliac graft with two curved cortical walls and a cancellous internal part.
grafting procedures were performed according to a standard protocol. The patients were given an intravenous antibiotic regimen (clindamycin 600 mg) during the operation and oral antibiotics postoperatively (clindamycin 300 mg three times a day) for 7 days. All patients remained hospitalized for 2e3 days. The iliac sutures were removed after 10 days. All patients were clinically evaluated after 1, 3, 10, and 30 days as well as after 3 and 6 months. The clinical evaluation included assessment of complications such as inflammation, mucosal erythema, wound dehiscences, and loss of bone grafts. Standardized radiographic examinations (orthopantomograms) were performed before and immediately after the surgical procedure, after 1, 3, 5, and 10 years. 2.4. Implant placement
2.3. Surgical procedure Surgery for bone augmentation and implant placement was performed under general anesthesia. The harvesting of the iliac graft was performed as described (Fretwurst et al., submitted for publication). After removal of the corticocancellous bone block from the inner table, additional cancellous bone was harvested with curettes. Ideally the harvested bone has a curved cortical wall and a cancellous internal part (Fig. 1). The size and contour of onlay grafts were limited to the size needed for an appropriate implant length (height, 9e16 mm). Intraorally, a slightly palatal crestal incision along the edentulous alveolar crest with distal and median vertical releasing incisions was performed, and a mucoperiosteal flap was raised. In cases with a combination of onlay graft and sinus elevation procedures, a standard sinus floor elevation was performed with cancellous bone (Boyne and James, 1980). The corticocancellous bone blocks were contoured and fixed to the labial and occlusal aspect of the alveolar ridge, so that the cortical wall faces occlusal and vestibular. Each bone block was secured with multiple microscrews (Modus 1.5; Medartis, Umkirch, Germany). The mucoperiosteal flap was passively mobilized and closed with a running suture and secured with four to five interrupted sutures (5-0 Monocryl; Ethicon, Norderstedt, Germany). All bone
After a healing period of 3 months, the previous incision line used in the grafting procedure was used for the preparation of a mucoperiosteal flap to remove the microscrews and to place the dental implants. Among all 32 patients, a total of 150 implants were placed according to the manufacturer's surgical protocol; 99 were Camlog RootLine implants (Camlog Biotechnologies, Wimsheim, Germany), 28 were Straumann Tissue Level implants (Straumann AG, Basel, Switzerland), and 23 were Steri-Oss implants (Nobel Biocare Deutschland GmbH, Cologne, Germany). The Camlog and Steri-Oss implants were inserted equicrestally. All Straumann implants were placed with the smootherough border at the crestal bone level. The mucoperiosteal flaps were closed with a running suture and secured with random interrupted sutures (5-0 Monocryl, Ethicon, Norderstedt, Germany). The time of unloaded healing of the implants was 12 weeks for maxillary implants and 8 weeks for mandibular implants. At loading, the stability of the implant was reassessed using a torque ratchet. If the torque value of the implant was >35 Ncm, then the prosthetic treatment was initialized. All patients received splinted prosthetic treatment. The patients were either restored with removable dentures seated on individually fabricated bars or with fixed bridges.
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
2.5. Radiographic evaluation All patients received spaced standardized radiological examination for evaluation of peri-implant crestal bone loss. The quantitative evaluation of the crestal bone loss was analyzed on routinely taken orthopantomographs as described previously mez-Roman et al., 1997; Semper et al., 2010; Heberer et al., (Go 2011; Nack et al., 2014). Conventional radiographs (Orthophos Plus, Sirona, Bensheim, Germany) were not digitized and were analyzed using a previously published method (Semper et al., 2010; Heberer et al., 2011). Digital orthopantomographs (Orthophos XG 5/Ceph, Sirona, Bensheim, Germany) were analyzed with Kodak Dental Imaging Software 6.8 (Carestream Dental, Stuttgart, Germany). The measurements of the vertical changes in the marginal bone were performed at described time points t0 (postoperatively ¼ baseline), t1 (after 1 year), t2 (after 3 years), t3 (after 5 years), and t4 (after 10 years) five times at the mesial (m) and distal (d) sites of the implant. To eliminate radiographic distortions, the values were adjusted with respect to the original length of the implant. The interpretation of the values of the mesial and distal sites was performed separately, and the mean values for all sites (mesial/ distal) were determined as follows: m1/d1 ¼ value of mesial/distal bone contact from the reference point after 1 year; m2/d2 ¼ value of mesial/distal bone contact from the reference point after 3 years; m3/d3 ¼ value of mesial/distal bone contact from the reference point after 5 years; and m4/d4 ¼ value of mesial/distal bone contact from the reference point after 10 years. Bone level changes were analyzed by subtracting the values of bone loss from the initial postoperative value. 2.6. Statistical analysis The intraclass correlation coefficient (ICC) was used to determine the intraobserver reliability using SPSS 16.0 software (SPSS Inc., Chicago, IL, USA). Besides the descriptive evaluation of the data, the correlations between diameter, age, gender, and localization with mesial and distal bone level changes were analyzed using the ManneWhitney U-test and the Spearman rank-order correlation coefficient. The mesial and distal sites were analyzed separately. Statistical analyses were performed using the SPSS 13.0 software (SPSS Inc.) and SAS, Version 9.1 (SAS Institute Inc., Cary, NC, USA). A p-value of <0.05 was considered statistically significant.
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Table 1 Data for crestal bone loss at all implants over an observation period of up to 120 months. Bone level (mm) t1 Maxillary Mandible Mesial Distal
0.9 1.0 0.8 0.9
t2 (0e3.5) (0e2.2) (0e3) (0e4)
1.4 1.1 1.4 1.4
t3 (0.1e3.8) (0.2e2.7) (0e4) (0.1e4)
1.7 1.8 1.8 1.7
t4 (0.1e4.0) (0.5e2.9) (0e4) (0.2e4)
1.8 (0.4e4.0) 1.8 (0.5e4) 1.8 (0.5e4)
Baseline: t1, 1 year; t2, 3 years; t3, 5 years; t4, 10 years. Table 2 Data for crestal bone loss at all implants over an observation period of more than 60 months. Bone level (mm)
Mesial Distal
t1
t2
t3
t4
0.9 0.8
1.4 1.4
1.8 1.7
1.8 1.8
Baseline: t1, 1 year; t2, 3 years; t3, 5 years; t4, 10 years.
0.5e4 mm) and in male patients a mean bone level change of 1 mm (range, 0.5e2 mm) were documented after 10 years. Of all implants, 92 had a follow-up of 5 or more years; mean values of bone level changes of this observation period are listed in Table 2. Statistical analysis showed that there was a significant difference between genders (Pmesialþdistal<0.01) regarding the crestal bone loss after 10 years, but no significant difference was found between the diameter of the implants (Pmesial ¼ 0.26, Pdistal ¼ 0.68), implant systems (Pmesial ¼ 0.37, Pdistal ¼ 0.15), and age (Pmesial ¼ 0.13, Pdistal ¼ 0.68) (Fig. 2). Length, diameter, frequency, and manufacturer of the implant systems used are shown in Table 3. 4. Discussion The present study demonstrates that patients with atrophied jaws can undergo sufficient reconstruction with current dental
3. Results A total of 150 implants were placed (23 Steri-Oss, 99 Camlog and 28 Straumann). The mean observation period of all implants was 69 months (range, 12e165 months). A total of 88 implants (maxilla, 83, mandible, 5) were followed up for more than 5 years, and 29 implants were followed up for an observation period of 13 years. The mean observation period of the maxilla with 125 implants (23 Steri-Oss, 82 Camlog implants, 20 Straumann) was 75 months (range, 12e165 months) and of the mandible with 25 implants (17 Camlog implants, 8 Straumann implants); the mean follow-up was 42 months (range, 12e91 months). During the observation period, seven implants (5 maxillary and 2 mandibular implants) were lost. Two implants in the lower jaw were lost prior to loading due to a failed osseointegration. No second implant insertion was performed. One implant was lost in the maxilla after 6 years and four maxillary implants after 8 years due to peri-implantitis. The survival rate of the implants was 95% (maxilla, 96%; mandible, 92%). The mean values of bone level changes over time are listed in Table 1. In female patients a mean crestal bone loss of 2 mm (range,
Fig. 2. Box-plot showing the significant difference of the crestal bone loss between the gender after ten years (M-Male, F-Female, mesialemesial implant site, distaledistal implant site).
Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037
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T. Fretwurst et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e5
Table 3 Lengths, diameters, frequencies, and manufacturers of the implant systems used. System
Diameter
Frequency
%
Steri-Oss
3,3 3,8 4,5 Total 3,8 4,3 5,0 6,0 Total 3,3 4,1 Total
4 14 5 23 63 33 2 1 99 2 26 28
17.4 60.9 21.7 100.0 63.4 33.3 2.0 1.0 100.0 7.1 92.9 100.0
Camlog
Straumann
System
Length
Frequency
%
Steri-Oss
10 12 14 16 Total 9 11 13 16 Total 10 12 Total
1 14 4 4 23 4 45 45 5 99 17 11 28
4.3 60.9 17.4 17.4 100.0 4.0 45.5 45.5 5.0 100.0 60.7 39.3 100.0
Camlog
Straumann
implant systems after iliac onlay bone grafting with an overall implant survival rate of 95% in the long term. The longest observation period was 13 years. The present implant survival rates are comparable with other long-term follow-up studies. The implant survival rates were 98.7% after 5.5 years, 100% up to 6 years, 96.7% after 9 years, and 100% after 10 years (patient collective range, 13e40) (Verhoeven et al., 2006; Chiapasco et al., 2008; Sbordone et al., 2012; Boven et al., 2014). In the 1970s, iliac crest augmentation was used only to improve prosthetic rehabilitation without implant insertion, resulting in an almost complete resorption of the autogenous graft (Curtis et al., 1977). The one-step technique (bone augmentation with immediate implant insertion) showed problems comprising insufficient implant positioning for prosthetic rehabilitation and tissue dehiscence (Nystrom et al., 1993). At the end of the 1990s, the two-stage method was established, with a 6-month healing period for the iliac graft (Lundgren et al., 1997). Since then, the timing of implant placement, whether simultaneous or delayed, has been discussed € stro €m et al., in the literature extensively (Lundgren et al., 1997; Sjo 2006; Verhoeven et al., 2006). There are a few long-term studies after iliac crest grafting evaluating the peri-implant bone level €stro € m et al. 2007; changes with a graft healing time of 6 months (Sjo €m et al., 2009). Other studies showed that 3 months of Nystro healing both for the graft and the implants is sufficient for the revascularization of the graft and the secure insertion of roughsurfaced dental implants as well as the loading of the implants (Nelson et al., 2006a,b; Heberer et al., 2009; Semper et al., 2010). In this study, the two-step technique with an implant insertion after 3 months was applied because several authors reported better implant integration and positioning with this approach (Lundgren € stro €m et al., 2006). The success rates in this study et al., 1997; Sjo justify this concept and healing period. In the present study, the major crestal bone loss appears within the first year. On average, less than 1 mm is lost in the first year. This is observed in implants placed in avascular fibula grafts and in nonaugmented regions as well. The results within this study demonstrate that the implants placed in augmented bone revealed
similar bone level changes compared to implants inserted in nonaugmented regions (Jemt et al., 1996; Nelson et al., 2006a,b; Semper et al., 2010). Several authors of comparable studies did not measure the periimplant bone level after implant insertion (Verhoeven et al., 2006; Sbordone et al., 2012). Data from Boven et al. are difficult to compare, as only an accumulated mean radiographic marginal bone loss (0.6 ± 0.7 mm) is shown at least after 5 years (Boven et al., 2014). Chiapasco et al. confirm the present data; there is also approximately 1 mm peri-implant bone loss detected after 1 year. After 5 years, still 1 mm is lost. However, the aforementioned study is limited: Only the lower jaw was examined, and in the period between loading and recall after 10 years, the number of implants was halved (Chiapasco et al., 2008). Strategies to minimize bone resorption after autogenous grafting are discussed in the literature (Cordaro et al., 2011; Wiltfang et al., 2014). The additional application of deproteinized bovine bone matrix (DBBM) has been shown to reduce bone resorption of autogenous grafts (Maiorana et al., 2005; Wiltfang et al., 2005; Maestre-Ferrin et al., 2009; Cordaro et al., 2011; Wiltfang et al., 2014). A cohort study with similar defect sizes, age, and gender distribution showed that DBBM coverage of the iliac crest graft reduced the early bone resorption (12 months) postoperatively, but long-term data are missing (Wiltfang et al., 2014). The age of the patient or implant system used had no impact on the survival rate or crestal bone loss, whereas gender seemed to be of importance. Females showed significantly more marginal bone loss than males after 10 years. This might be due to a difference in individual factors influencing bone physiology. Estrogens and androgens are discussed in bone health and preservation (Manolagas et al., 2013). The sex steroid hormones maintain a balance between bone formation and resorption through changes in osteoclastogenesis and osteoblastogenesis (Manolagas et al., 2013). The interindividual, gender-specific hormone status may play a role in bone physiology of oral autologous grafts. However, further studies are necessary to identify factors influencing bone resorption. In previous studies, often only survival rates were documented as parameters of success; however, peri-implant bone loss rates should be considered as well. 5. Conclusion The reconstruction of atrophic jaws with cortico-cancellous bone grafts from the anterior superior iliac crest and placement of endosseous implants is a predictable technique to facilitate longterm rehabilitation of the extremely atrophic jaw. The mean periimplant bone loss is comparable to that found in nonaugmented bone. The overall implant survival rate exceeds 95%. Conflict of interest The authors reported no conflicts of interest related to this study. Acknowledgment This study was partially funded by the Camlog Foundation (CF41306). References €ndahl K, Brånemark PI, Lindstro € m J, Jacobsson M: ReconAdell R, Lekholm U, Gro struction of severely resorbed edentulous maxillae using osseointegrated fixtures in immediate autogenous bone grafts. Int J Oral Maxillofac Implants 5(3): 233e246, 1990
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Please cite this article in press as: Fretwurst T, et al., Long-term retrospective evaluation of the peri-implant bone level in onlay grafted patients with iliac bone from the anterior superior iliac crest, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/ j.jcms.2015.03.037