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Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting
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JORMAS-798; No. of Pages 7 J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx
Available online at
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Original Article
Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting E. Cansiz a,d,*, J. Haq b, M. Manisali b, S. Cakarer d, B.A. Gultekin c a
Department of Oral and Maxillofacial Surgery, Faculty of Medicine, Istanbul University Istanbul, Istanbul, Turkey Department of Oral and Maxillofacial Surgery, Saint-George’s Medical Univerity, London, England, United Kingdom Department of Implantology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey d Faculty of dentistry, oral and maxillofacial surgery, Istanbul university, Istanbul, Turkey b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 18 August 2019 Accepted 20 November 2019
Purpose: The purpose of this study was to evaluate long-term three-dimensional graft resorption following reconstruction of the severely atrophic maxilla with anterior iliac crest bone grafting. Methods: Twenty-two patients (13 males), who underwent autogenous bone grafting and implant placement to their severely atrophic maxillary alveolar ridges were identified and included in the study. Pre- and postoperative cone-beam computed tomography (CBCT) scans of 40 recipient grafting sites were evaluated to calculate volumetric changes over time. CBCT scans were performed preoperatively (V0) and one week (V1), three months (V2), one year (V3), and three years (V4) following the augmentation operation. Results: The average graft resorption from V1 to V2, V1 to V3, and V1 to V4 was 31.42%, 33.96%, and 37.96%, respectively. Initial graft volume reduction within the first three months was statistically higher compared to other postoperative periods (P < 0.013). The rate of resorption reduced slightly from the third month of the surgery (V2) (P > 0.013). There was no statistical difference between resorption volume and gender, type of prosthesis, the presence of vestibuloplasty, or patient age (P > 0.05). Conclusion: The overall success rate of the iliac bone block grafts was found to be high. The volumetric resorption rates associated with the graft were favourable for the reconstruction of the maxilla and for permitting the placement of dental implants three months after augmentation. The highest graft resorption was found at the third postoperative month. Placement and loading of the implants reduced the resorption rate slightly over time.
C 2020 Elsevier Masson SAS. All rights reserved.
Keywords: Anterior iliac crest Bone graft Resorption
1. Introduction Maxillary dento-alveolar bone resorption following malignancy, trauma, congenitally missing teeth, oro-facial infections or atrophy secondary to tooth extraction may result in inadequate bone volume required for the placement and long-term success of dental implants [1]. Although there are many different techniques to provide sufficient bone volume for dental implantation, such as guided bone regeneration, ridge splitting techniques or distraction osteogenesis, autogenous bone grafting may be preferable due to its osteogenic potential [2,3]. Anterior iliac crest bone harvest and grafting is a wellknown and widely practised technique for the reconstruction of the severely atrophic maxilla in such instances [4,5]. * Corresponding author. E-mail address: [email protected] (E. Cansiz).
Anterior iliac crest bone grafting techniques maintain structurally sound maxillary alveolar process volume for dental implantation. However, variable resorption rates have been reported after such grafting [6–8]. The volumetric stability of the augmented site during the healing process serves as a measure of treatment success. Panoramic and other two-dimensional (2D) radiographic images inaccurately evaluate volumetric changes and imprecisely measure threedimensional (3D) changes [9]. In contrast, cone-beam computed tomography (CBCT) more accurately measures and evaluates the volume of the augmented site prior to implant placement [10]. Because of the perspectives mentioned above, we conducted this retrospective research to assess the 3D graft resorption rates after anterior iliac crest bone grafting performed for the reconstruction of the severely atrophic maxillary alveolar ridge and the main aim of this study was to determine the long-term character of bone resorption.
https://doi.org/10.1016/j.jormas.2019.11.004 C 2020 Elsevier Masson SAS. All rights reserved. 2468-7855/
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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2. Materials and methods 2.1. Study design Patients were identified who underwent surgery for the reconstruction of the atrophic maxillary alveolar ridge using grafted autologous anterior iliac crest bone from December 2011 to January 2014 at the Istanbul University, Departments of Oral Implantology and Oral and Maxillofacial Surgery retrospectively. Two patients were excluded because of inadequate image quality. Twenty-two patients (13 male) with 40 grafting sites of an age range of 28–64 years and a mean age of 49.59 10.06 years were included in the study. Specific inclusion criteria of the study were the initial presence of an atrophic maxillary alveolar ridge with a residual bone height of < 7 mm and/or width of < 4 mm that had been augmented with anterior iliac crest block graft and CBCT records preoperatively, as well as at one week and three, twelve and 36 months postoperatively. The exclusion criteria of the study were previous surgery at the recipient or donor site, contraindicating metabolic diseases, chronic periodontal disease and/or tobacco usage. Declaration of Helsinki on medical protocol and ethics were followed in this study and the research was approved by the Regional Ethical Review Board of Istanbul University (Protocol No. 2015/61). All of the patients who participated in the study signed an informed consent agreement. 2.2. Surgical methods Following intraoral, extraoral, and radiological examination, patients were selected to undergo anterior iliac crest block bone grafting to reconstruct the severely atrophic maxillary ridge. Following the induction of anesthesia, a split thickness sulcular
incision was performed in the maxillary labial vestibule and submucosal layers were separated by blunt dissection. After the dissection, a periosteal incision was performed and a mucoperiosteal flap was elevated to the crest of the alveolar bone. The recipient site was measured to calculate the volume required to reconstruct the alveolar bone and the conventional grafting technique was performed to harvest bone graft from anterior iliac crest. Following cutaneous incision on the anterosuperior iliac spine, subcutaneous soft tissues, muscle attachments, and periosteum were dissected to reach the anterior iliac crest. After the exposure of the anterior iliac crest, a tricortical (corticocancellous) bone block was harvested using a microsaw under sterile saline irrigation. Cancellous chips were curretted from residual donor site. Any sharp edges of the donor site were smoothed with rotary tools and the wound was closed in a layers. A mini-vac drain was sited and secured to prevent hematoma formation (Fig. 1a–d). Following the bone harvesting procedure, the block bone graft was reshaped and adapted to fit the recipient site anatomy. Eleven to 15 mm long 2.0 mm in diameter titanium screws (KLS Martin, Germany) were used to fix the bone grafts to the residual alveolar ridge to avoid micro movements during the integration period (Fig. 2a and b). The sharp edges of the bone grafts were smoothed using round diamond burs to avoid graft exposure during the healing period. No additional membranes or bone grafting biomaterials were used for the reconstruction. The flap of the recipient site was sutured via simple and mattress nonabsorbable sutures (Dogsan Medical Supplies Industry, Trabzon, Turkey). Non-resorbable sutures were removed 7–10 days following surgery and the patients were recalled monthly for the initial three months of the graft integration period. The success of the bone grafting was determined by absence of infection, graft exposure and/or radiolucency on the postoperative
Fig. 1. Anterior iliac crest bone graft harvesting. a. Osteotomies performed via microsaw. b. Tricortical autogenous block bone graft. c. Segmentation of the bone graft. d. Placement of mini-vac drain and primary closure of the donor site.
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 2. Pre- and postoperative appearance of the recipient site. a. Preoperative view of severely atrophic maxilla. b. Adaptation and fixation of the block grafts. c. Appearance of the recipient site after graft integration. d. Placement of the dental implants.
CBCT data and the identification of revascularisation during dental implantation and immobility of the integrated grafts at the recipient bed [11]. At the end of the three-month graft integration period, it was observed that no additional grafting procedure was required for any of the patients and the dental implantations were performed (Fig. 2c and d). Temporary prostheses were not permitted during the graft and implant integration periods. Vestibuloplasty was performed to increase the sulcular depth in 15 patients. After a further three months, patients underwent prosthodontic rehabilitation. Porcelain-fused-to-metal, cementretained, fixed crowns, or bridges were fabricated and fitted. Implant at success was evaluated at this time point. 2.3. Radiographic analysis Pre- and postoperative CBCT scans were obtained to calculate volumetric changes at the grafted site. Before the study, the intraexaminer study error was calculated using postoperative images from 10 randomly selected augmented sites. The same investigator, who was not involved in performing the operations, repeated the measurements with excellent reliability (R = 0.960). CBCT was performed before (V0) and one week (V1), three months (V2), one year (V3), and three years (V4) after the augmentation operation. Scans were evaluated by using the i-CAT 3D Imaging System (Imaging Sciences International, Hatfield, PA, USA) with a field of view of 13 8 cm and a 0.25 voxel size. Data obtained from the CBCT images of augmented sites were transferred to a network computer workstation where graft volumetric changes were analyzed using MIMICS 14.0 software (Materialise Europe, Leuven, Belgium). Radiological appearance of the dental implants and prosthodontics were cleaned from V3 and V4 DICOM data to avoid radiologic artifacts by using the ‘‘Edit Masks’’ tool of the MIMICS software. The digital volumetric calculation methodology has been described in previous publications [12,13]. Digital reconstruction was accomplished by selecting the grafted volume and was manually performed with a threshold value determined by the gray values of native bone and grafted bone expressed on CBCT images. In order to ensure the reproducibility of volumetric
measurements at V1, V2, V3, and V4, the grafted sites was selected with reference to anatomic landmarks and the bone fixation screws. After selection of the grafted sites, 3D reconstruction was achieved using the 3D calculation tool of MIMICS (Fig. 3a and b). 2.4. Statistics Statistical significance analysis was carried out by using SPSS software (Version 21.0; SPSS; Chicago, IL, USA). The level of significance was set at 0.05 (P < 0.05). Shapiro–Wilk test was performed to test the normalisation of the data. Since the normal distribution of the data could not be verified (P < 0.05), statistically significant differences among the volumes of grafted donor sites and the amount of grafted iliac bone resorption over the postoperative periods were determined using the non-parametric Friedman’s ANOVA test. Mann–Whitney U post-hoc test was implemented to determine the significant difference between paired groups. The differences between paired groups for volume of grafted donor site and amount of the grafted iliac bone resorption were evaluated at the levels of significance of 0.013 (P < 0.013) and 0.017 (P < 0.017), respectively. In addition, the relationships between the bone resorption volume and gender, the presence of vestibuloplasty, and age were also analyzed statistically using Mann–Whitney U test (P < 0.05). 3. Results Minor complications including postoperative pain, superficial infection of the donor site (1 subject), and temporary neurosensory disturbance (2 subjects) were recorded during the three-month graft integration period. Following this stage, a total of 135 dental implants (Biohorizons, Birmingham, USA) were placed to permit prosthodontic rehabilitation. Three of 135 dental implants failed after loading (97.8% survival rate). The average follow-up period was 30.27 months ( 8.72 months, range 12–40 months) (Fig. 4). Initial average graft volume was 6305.45 mm3 (V1). This decreased to 4324.47 mm3 (31.42%) (V2), 4164.13 mm3 (33.96%) (V3) and 3912.07 mm3 (37.96%) (V4) (Fig. 5). Initial graft volume reduction within the first three months (between V1 and V2) was
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 3. a. 3D reconstruction and calculation of graft volume by using computer software. 3D calculation of preoperative (V0) bone volume. b. 3D reconstruction of V1, V2, V3 and V4 bone volumes.
statistically higher than those calculated between V2 and V3, and V3 and V4 (P < 0.013). The amount of resorption reduced slightly over time from the third month of the surgery (V2) (P > 0.013) (Fig. 5). Average graft resorption volumes were 1980.98 mm3 (V1 to V2), 2141.32 mm3 (V1 to V3) and 2393.38 mm3 (V1 to V4). Differences between V1 and V2, and V1 and V4 were statistically significant (P < 0.017) (Fig. 6). There was no statistical difference between resorption volume and gender, the presence of vestibuloplasty, or age (P > 0.05).
4. Discussion Graft stability, the vascularity of the recipient bed, and the osteogenic potential of the grafted bone are important factors which affect bone graft survival. Block grafts with cortical bone are preferable to provide rigidity for fixation and to prevent bony resorption, although cortical bone grafts impair the integration of the graft due to the poor vascularization. Cortico-cancellous blocks harvested from the iliac crest provide both the mechanical advantages of the cortical bone and the biological advantages of the cancellous bone [14] as employed in this study. Barone and Covani [15] evaluated the clinical success of bony reconstruction of the severely atrophic maxilla using autogenous iliac crest for vertical and horizontal augmentation. They reported that the failure rate for vertical augmentation was higher than horizontal augmentation. In the present study, all grafts were fully integrated and no complications of graft exposure or failure associated with horizontal or vertical augmentation was observed at the recipient site according the data evaluated during the study period. The stable fixation of the graft and tension-free primary closure of the soft tissue flaps aimed to provide optimal graft healing during the study period.
Anterior or posterior approaches have been used to harvest iliac crest graft. Orthopaedic and neurosurgeons favour the posterior approach to harvest an iliac crest graft. This approach has been associated with sacroiliac joint instability [6]. Maxillofacial surgeons generally prefer the anterior approach as presented in this study. Despite the anterior approach generally being recognised as a procedure with low donor site morbidity, some minor complications have been reported including gait disturbance, paresthesia, hematomas, superficial infections, and pain [6,16]. In our study, temporary sensory disturbance was observed in two patients. Gait disturbances and pain resolved within three weeks, which is in agreement with the results reported by Barone and Cavani [15]. One patient had a superficial infection which was managed by local and systemic antibiotic treatment. More prospective studies are needed to compare the anterior and posterior approach regarding the incidence and severity of postoperative morbidity. Some authors suggest using barrier membranes to reduce quantitative and qualitative resorption of the autogenous block grafts. Monje et al. reported that the use of absorbable collagen membrane is a predictable technique for augmenting anterior maxillary horizontal ridge deficiency [17]. In the present study, no barrier membranes were utilised, and no problems associated with graft integration or bone healing were observed. No adequate clinical data is available regarding the use of membranes in promoting bone regeneration in iliac crest graft augmentation and there is insufficient evidence that the use of barrier membranes prevent the resorption of autogenous onlay block grafts [14]. Volumetric stability of the augmented site is important for the success of the treatment. It is not possible to make a proper evaluation using 2D radiographic techniques. Therefore we aimed to include the data of the 3D results of volume changes of the grafted regions in this study. Various resorption rates of iliac bone grafts have been reported in the literature by using 2D and 3D
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 4. Descriptive summary of the study.
techniques. Vermeeren et al. [18] evaluated resorption by using panoramic radiographs and reported an overall bone resorption rate approaching 50%. The authors did not recommend this technique due to the bone resorption occurring in an unpredictable way. In a CT-based research, Nystrom et al. [19] demonstrated that overall reduction of the graft was about 50% after one year of augmentation. In this research, the implants were placed at the same time with the large, horseshoe-shaped grafts from the iliac crest. Johansson et al. [20] evaluated the changes in volume of autogenous iliac crest grafted as onlay or inlay in the maxilla by using CT. They reported the resorption of 50% for onlay corticocancellous autogenous grafts 6 month after augmentation. Sbordone et al. [21] evaluated CT scan data of the patients who underwent iliac graft surgery. They reported that the average
resorption was 42% when the onlay was positioned in the anterior maxilla and 16% if it was positioned in the posterior maxilla one year following implant placement. Dreisidler et al. [22] reported the most favorable results regarding the resorption rate (15%) associated with iliac bone grafts. The resorption rates were found lower than those reported by Nystrom et al. [19] and Johansson et al. [20], but higher than those reported by Dreisidler et al. [22]. The differences may be attributed to the different surgical techniques of harvesting. Sbordone et al. reported that implant loading may slow volume resorption [21]. In our study, the resorption rate was found as 31.42% three months after augmentation (V2), 33.96% one year after augmentation (V3), and 37.96% three years after augmentation (V4). The most important finding of the present study is that
Fig. 5. Average volumes of grafted donor sites measured during the cone-beam computed tomography (CBCT) evaluations periods. V0: preoperative period; V1: postoperative first week; V2: postoperative third month before implant surgery; V3: postoperative first year; V4: postoperative third year; *: denotes statistically significant difference among volumes of grafted donor sites (P < 0.013).
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Figure 6. Average ( standard deviation) amount of the grafted iliac bone resorption. *: denotes the statistically significant difference between resorption volumes.
the resorption rates reduced significantly with time. The implants were placed three months after augmentation and loaded three months after the placement. Therefore, we may suggest that early implant placement and loading may reduce bone resorption rates over time in iliac grafting procedures. The mechanism associated with bone graft resorption is still not clearly understood [15]. In our study, we did not find any statistically significant relationship between resorption volume and gender, the presence of concurrent vestibuloplasty, and patient age. Johansson et al. suggested that a greater initial graft volume correlated with higher resorption rates [20]. In our study, we harvested tricortical large cortico-cancellous iliac block bone grafts. According to our results, we cannot agree with the suggestion reported by Johansson et al. [20] Higher resorption rates in large grafts might be associated with the increasing difficulties of ensuring primary closure which needs careful release of the soft tissue as reported by Dreiseidler et al. [22] In our study, despite the placement of large cortico-cancellous graft, no exposure of the graft was observed because of the passive closure of the mucosa at the recipient site. Dental implant placement and success pose challenges in the case of the severely resorbed maxilla. The reasons for multiple implant failures in grafted bone are important, and local and systemic factors may influence the implant survival rate [23]. Barone and Covani [15] reported the implant failure rate as 5.1% in severely resorbed maxillae grafted with anterior corticocancellous iliac crest. All implant failures occurred during the first six months after placement and prior to implant loading. There are still controversies regarding the time of the placement of the implants at the grafted area. Despite a one-stage protocol reducing the number of surgical procedures, most clinicians suggest performing a two-stage protocol [24–26]. The present study demonstrated the results of a two-stage approach. Three of 135 dental implants used for prosthodontic rehabilitations failed after loading (97.8% survival rate). Two of the failed implants were placed at the posterior maxilla and the third implant was placed at the anterior maxilla. There was no systemic disease history or smoking habit in the patients who suffered implant failure. Therefore, the failures may have been associated with the reduced bone volume at the surgical sites of the implants. The survival rate of the implants was found slightly higher than those reported by Barone and Covani [15] and Pereira et al. [14] and slightly lower than those reported by Sbordone et al. [21].
5. Conclusion The success rate of the iliac bone block grafts was found to be high. The volumetric resorption rates associated with the graft were favourable for the reconstruction of the atrophic maxilla and for permitting the insertion of dental implants three months following augmentation. The highest graft resorption was found in the third postoperative month. Placement and loading of the implants reduced the resorption rate slightly over time. Disclosure of interest The authors declare that they have no competing interest.
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[20] Johansson B, Grepe A, Wannfors K, et al. A clinical study of changes in the volume of bone grafts in the atrophic maxilla. Dentomaxillofac Radiol 2001;30:157–61. [21] Sbordone L, Toti P, Menchini-Fabris GB, et al. Volume changes of autogenous bone grafts after alveolar ridge augmentation of atrophic maxillae and mandibles. Int J Oral Maxillofac Surg 2009;38(10):1059–65. [22] Dreiseidler T, Kaunisaho V, Neugebauer J, et al. Changes in volume during the four months’ remodelling period of iliac crest grafts in reconstruction of the alveolar ridge. Br J Oral Maxillofac Surg 2016;54(7):751–6. [23] Sjo¨stro¨m M, Sennerby L, Lundgren S. Bone graft healing in reconstruction of maxillary atrophy. Clin Implant Dent Relat Res 2013;15(3):367–79. [24] Lundgren S, Rasmusson L, Sjostrom M, et al. Simultaneous or delayed placement of titanium implants in free autogenous iliac bone grafts. Int J Oral Maxillofac Surg 1999;28:31. [25] Lundgren S, Rasmusson L, Sjostrom M, et al. 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. [26] Sjostrom M, Lundgren S, Sennerby L. A histomorphometric comparison of the bone graft-titanium interface between interpositional and onlay/inlay bone grafting technique. Int J Oral Maxillofac Implants 2006;21:52.
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
JORMAS-798; No. of Pages 7 J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx
Available online at
ScienceDirect www.sciencedirect.com
Original Article
Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting E. Cansiz a,d,*, J. Haq b, M. Manisali b, S. Cakarer d, B.A. Gultekin c a
Department of Oral and Maxillofacial Surgery, Faculty of Medicine, Istanbul University Istanbul, Istanbul, Turkey Department of Oral and Maxillofacial Surgery, Saint-George’s Medical Univerity, London, England, United Kingdom Department of Implantology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey d Faculty of dentistry, oral and maxillofacial surgery, Istanbul university, Istanbul, Turkey b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 18 August 2019 Accepted 20 November 2019
Purpose: The purpose of this study was to evaluate long-term three-dimensional graft resorption following reconstruction of the severely atrophic maxilla with anterior iliac crest bone grafting. Methods: Twenty-two patients (13 males), who underwent autogenous bone grafting and implant placement to their severely atrophic maxillary alveolar ridges were identified and included in the study. Pre- and postoperative cone-beam computed tomography (CBCT) scans of 40 recipient grafting sites were evaluated to calculate volumetric changes over time. CBCT scans were performed preoperatively (V0) and one week (V1), three months (V2), one year (V3), and three years (V4) following the augmentation operation. Results: The average graft resorption from V1 to V2, V1 to V3, and V1 to V4 was 31.42%, 33.96%, and 37.96%, respectively. Initial graft volume reduction within the first three months was statistically higher compared to other postoperative periods (P < 0.013). The rate of resorption reduced slightly from the third month of the surgery (V2) (P > 0.013). There was no statistical difference between resorption volume and gender, type of prosthesis, the presence of vestibuloplasty, or patient age (P > 0.05). Conclusion: The overall success rate of the iliac bone block grafts was found to be high. The volumetric resorption rates associated with the graft were favourable for the reconstruction of the maxilla and for permitting the placement of dental implants three months after augmentation. The highest graft resorption was found at the third postoperative month. Placement and loading of the implants reduced the resorption rate slightly over time.
C 2020 Elsevier Masson SAS. All rights reserved.
Keywords: Anterior iliac crest Bone graft Resorption
1. Introduction Maxillary dento-alveolar bone resorption following malignancy, trauma, congenitally missing teeth, oro-facial infections or atrophy secondary to tooth extraction may result in inadequate bone volume required for the placement and long-term success of dental implants [1]. Although there are many different techniques to provide sufficient bone volume for dental implantation, such as guided bone regeneration, ridge splitting techniques or distraction osteogenesis, autogenous bone grafting may be preferable due to its osteogenic potential [2,3]. Anterior iliac crest bone harvest and grafting is a wellknown and widely practised technique for the reconstruction of the severely atrophic maxilla in such instances [4,5]. * Corresponding author. E-mail address: [email protected] (E. Cansiz).
Anterior iliac crest bone grafting techniques maintain structurally sound maxillary alveolar process volume for dental implantation. However, variable resorption rates have been reported after such grafting [6–8]. The volumetric stability of the augmented site during the healing process serves as a measure of treatment success. Panoramic and other two-dimensional (2D) radiographic images inaccurately evaluate volumetric changes and imprecisely measure threedimensional (3D) changes [9]. In contrast, cone-beam computed tomography (CBCT) more accurately measures and evaluates the volume of the augmented site prior to implant placement [10]. Because of the perspectives mentioned above, we conducted this retrospective research to assess the 3D graft resorption rates after anterior iliac crest bone grafting performed for the reconstruction of the severely atrophic maxillary alveolar ridge and the main aim of this study was to determine the long-term character of bone resorption.
https://doi.org/10.1016/j.jormas.2019.11.004 C 2020 Elsevier Masson SAS. All rights reserved. 2468-7855/
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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2. Materials and methods 2.1. Study design Patients were identified who underwent surgery for the reconstruction of the atrophic maxillary alveolar ridge using grafted autologous anterior iliac crest bone from December 2011 to January 2014 at the Istanbul University, Departments of Oral Implantology and Oral and Maxillofacial Surgery retrospectively. Two patients were excluded because of inadequate image quality. Twenty-two patients (13 male) with 40 grafting sites of an age range of 28–64 years and a mean age of 49.59 10.06 years were included in the study. Specific inclusion criteria of the study were the initial presence of an atrophic maxillary alveolar ridge with a residual bone height of < 7 mm and/or width of < 4 mm that had been augmented with anterior iliac crest block graft and CBCT records preoperatively, as well as at one week and three, twelve and 36 months postoperatively. The exclusion criteria of the study were previous surgery at the recipient or donor site, contraindicating metabolic diseases, chronic periodontal disease and/or tobacco usage. Declaration of Helsinki on medical protocol and ethics were followed in this study and the research was approved by the Regional Ethical Review Board of Istanbul University (Protocol No. 2015/61). All of the patients who participated in the study signed an informed consent agreement. 2.2. Surgical methods Following intraoral, extraoral, and radiological examination, patients were selected to undergo anterior iliac crest block bone grafting to reconstruct the severely atrophic maxillary ridge. Following the induction of anesthesia, a split thickness sulcular
incision was performed in the maxillary labial vestibule and submucosal layers were separated by blunt dissection. After the dissection, a periosteal incision was performed and a mucoperiosteal flap was elevated to the crest of the alveolar bone. The recipient site was measured to calculate the volume required to reconstruct the alveolar bone and the conventional grafting technique was performed to harvest bone graft from anterior iliac crest. Following cutaneous incision on the anterosuperior iliac spine, subcutaneous soft tissues, muscle attachments, and periosteum were dissected to reach the anterior iliac crest. After the exposure of the anterior iliac crest, a tricortical (corticocancellous) bone block was harvested using a microsaw under sterile saline irrigation. Cancellous chips were curretted from residual donor site. Any sharp edges of the donor site were smoothed with rotary tools and the wound was closed in a layers. A mini-vac drain was sited and secured to prevent hematoma formation (Fig. 1a–d). Following the bone harvesting procedure, the block bone graft was reshaped and adapted to fit the recipient site anatomy. Eleven to 15 mm long 2.0 mm in diameter titanium screws (KLS Martin, Germany) were used to fix the bone grafts to the residual alveolar ridge to avoid micro movements during the integration period (Fig. 2a and b). The sharp edges of the bone grafts were smoothed using round diamond burs to avoid graft exposure during the healing period. No additional membranes or bone grafting biomaterials were used for the reconstruction. The flap of the recipient site was sutured via simple and mattress nonabsorbable sutures (Dogsan Medical Supplies Industry, Trabzon, Turkey). Non-resorbable sutures were removed 7–10 days following surgery and the patients were recalled monthly for the initial three months of the graft integration period. The success of the bone grafting was determined by absence of infection, graft exposure and/or radiolucency on the postoperative
Fig. 1. Anterior iliac crest bone graft harvesting. a. Osteotomies performed via microsaw. b. Tricortical autogenous block bone graft. c. Segmentation of the bone graft. d. Placement of mini-vac drain and primary closure of the donor site.
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 2. Pre- and postoperative appearance of the recipient site. a. Preoperative view of severely atrophic maxilla. b. Adaptation and fixation of the block grafts. c. Appearance of the recipient site after graft integration. d. Placement of the dental implants.
CBCT data and the identification of revascularisation during dental implantation and immobility of the integrated grafts at the recipient bed [11]. At the end of the three-month graft integration period, it was observed that no additional grafting procedure was required for any of the patients and the dental implantations were performed (Fig. 2c and d). Temporary prostheses were not permitted during the graft and implant integration periods. Vestibuloplasty was performed to increase the sulcular depth in 15 patients. After a further three months, patients underwent prosthodontic rehabilitation. Porcelain-fused-to-metal, cementretained, fixed crowns, or bridges were fabricated and fitted. Implant at success was evaluated at this time point. 2.3. Radiographic analysis Pre- and postoperative CBCT scans were obtained to calculate volumetric changes at the grafted site. Before the study, the intraexaminer study error was calculated using postoperative images from 10 randomly selected augmented sites. The same investigator, who was not involved in performing the operations, repeated the measurements with excellent reliability (R = 0.960). CBCT was performed before (V0) and one week (V1), three months (V2), one year (V3), and three years (V4) after the augmentation operation. Scans were evaluated by using the i-CAT 3D Imaging System (Imaging Sciences International, Hatfield, PA, USA) with a field of view of 13 8 cm and a 0.25 voxel size. Data obtained from the CBCT images of augmented sites were transferred to a network computer workstation where graft volumetric changes were analyzed using MIMICS 14.0 software (Materialise Europe, Leuven, Belgium). Radiological appearance of the dental implants and prosthodontics were cleaned from V3 and V4 DICOM data to avoid radiologic artifacts by using the ‘‘Edit Masks’’ tool of the MIMICS software. The digital volumetric calculation methodology has been described in previous publications [12,13]. Digital reconstruction was accomplished by selecting the grafted volume and was manually performed with a threshold value determined by the gray values of native bone and grafted bone expressed on CBCT images. In order to ensure the reproducibility of volumetric
measurements at V1, V2, V3, and V4, the grafted sites was selected with reference to anatomic landmarks and the bone fixation screws. After selection of the grafted sites, 3D reconstruction was achieved using the 3D calculation tool of MIMICS (Fig. 3a and b). 2.4. Statistics Statistical significance analysis was carried out by using SPSS software (Version 21.0; SPSS; Chicago, IL, USA). The level of significance was set at 0.05 (P < 0.05). Shapiro–Wilk test was performed to test the normalisation of the data. Since the normal distribution of the data could not be verified (P < 0.05), statistically significant differences among the volumes of grafted donor sites and the amount of grafted iliac bone resorption over the postoperative periods were determined using the non-parametric Friedman’s ANOVA test. Mann–Whitney U post-hoc test was implemented to determine the significant difference between paired groups. The differences between paired groups for volume of grafted donor site and amount of the grafted iliac bone resorption were evaluated at the levels of significance of 0.013 (P < 0.013) and 0.017 (P < 0.017), respectively. In addition, the relationships between the bone resorption volume and gender, the presence of vestibuloplasty, and age were also analyzed statistically using Mann–Whitney U test (P < 0.05). 3. Results Minor complications including postoperative pain, superficial infection of the donor site (1 subject), and temporary neurosensory disturbance (2 subjects) were recorded during the three-month graft integration period. Following this stage, a total of 135 dental implants (Biohorizons, Birmingham, USA) were placed to permit prosthodontic rehabilitation. Three of 135 dental implants failed after loading (97.8% survival rate). The average follow-up period was 30.27 months ( 8.72 months, range 12–40 months) (Fig. 4). Initial average graft volume was 6305.45 mm3 (V1). This decreased to 4324.47 mm3 (31.42%) (V2), 4164.13 mm3 (33.96%) (V3) and 3912.07 mm3 (37.96%) (V4) (Fig. 5). Initial graft volume reduction within the first three months (between V1 and V2) was
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 3. a. 3D reconstruction and calculation of graft volume by using computer software. 3D calculation of preoperative (V0) bone volume. b. 3D reconstruction of V1, V2, V3 and V4 bone volumes.
statistically higher than those calculated between V2 and V3, and V3 and V4 (P < 0.013). The amount of resorption reduced slightly over time from the third month of the surgery (V2) (P > 0.013) (Fig. 5). Average graft resorption volumes were 1980.98 mm3 (V1 to V2), 2141.32 mm3 (V1 to V3) and 2393.38 mm3 (V1 to V4). Differences between V1 and V2, and V1 and V4 were statistically significant (P < 0.017) (Fig. 6). There was no statistical difference between resorption volume and gender, the presence of vestibuloplasty, or age (P > 0.05).
4. Discussion Graft stability, the vascularity of the recipient bed, and the osteogenic potential of the grafted bone are important factors which affect bone graft survival. Block grafts with cortical bone are preferable to provide rigidity for fixation and to prevent bony resorption, although cortical bone grafts impair the integration of the graft due to the poor vascularization. Cortico-cancellous blocks harvested from the iliac crest provide both the mechanical advantages of the cortical bone and the biological advantages of the cancellous bone [14] as employed in this study. Barone and Covani [15] evaluated the clinical success of bony reconstruction of the severely atrophic maxilla using autogenous iliac crest for vertical and horizontal augmentation. They reported that the failure rate for vertical augmentation was higher than horizontal augmentation. In the present study, all grafts were fully integrated and no complications of graft exposure or failure associated with horizontal or vertical augmentation was observed at the recipient site according the data evaluated during the study period. The stable fixation of the graft and tension-free primary closure of the soft tissue flaps aimed to provide optimal graft healing during the study period.
Anterior or posterior approaches have been used to harvest iliac crest graft. Orthopaedic and neurosurgeons favour the posterior approach to harvest an iliac crest graft. This approach has been associated with sacroiliac joint instability [6]. Maxillofacial surgeons generally prefer the anterior approach as presented in this study. Despite the anterior approach generally being recognised as a procedure with low donor site morbidity, some minor complications have been reported including gait disturbance, paresthesia, hematomas, superficial infections, and pain [6,16]. In our study, temporary sensory disturbance was observed in two patients. Gait disturbances and pain resolved within three weeks, which is in agreement with the results reported by Barone and Cavani [15]. One patient had a superficial infection which was managed by local and systemic antibiotic treatment. More prospective studies are needed to compare the anterior and posterior approach regarding the incidence and severity of postoperative morbidity. Some authors suggest using barrier membranes to reduce quantitative and qualitative resorption of the autogenous block grafts. Monje et al. reported that the use of absorbable collagen membrane is a predictable technique for augmenting anterior maxillary horizontal ridge deficiency [17]. In the present study, no barrier membranes were utilised, and no problems associated with graft integration or bone healing were observed. No adequate clinical data is available regarding the use of membranes in promoting bone regeneration in iliac crest graft augmentation and there is insufficient evidence that the use of barrier membranes prevent the resorption of autogenous onlay block grafts [14]. Volumetric stability of the augmented site is important for the success of the treatment. It is not possible to make a proper evaluation using 2D radiographic techniques. Therefore we aimed to include the data of the 3D results of volume changes of the grafted regions in this study. Various resorption rates of iliac bone grafts have been reported in the literature by using 2D and 3D
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Fig. 4. Descriptive summary of the study.
techniques. Vermeeren et al. [18] evaluated resorption by using panoramic radiographs and reported an overall bone resorption rate approaching 50%. The authors did not recommend this technique due to the bone resorption occurring in an unpredictable way. In a CT-based research, Nystrom et al. [19] demonstrated that overall reduction of the graft was about 50% after one year of augmentation. In this research, the implants were placed at the same time with the large, horseshoe-shaped grafts from the iliac crest. Johansson et al. [20] evaluated the changes in volume of autogenous iliac crest grafted as onlay or inlay in the maxilla by using CT. They reported the resorption of 50% for onlay corticocancellous autogenous grafts 6 month after augmentation. Sbordone et al. [21] evaluated CT scan data of the patients who underwent iliac graft surgery. They reported that the average
resorption was 42% when the onlay was positioned in the anterior maxilla and 16% if it was positioned in the posterior maxilla one year following implant placement. Dreisidler et al. [22] reported the most favorable results regarding the resorption rate (15%) associated with iliac bone grafts. The resorption rates were found lower than those reported by Nystrom et al. [19] and Johansson et al. [20], but higher than those reported by Dreisidler et al. [22]. The differences may be attributed to the different surgical techniques of harvesting. Sbordone et al. reported that implant loading may slow volume resorption [21]. In our study, the resorption rate was found as 31.42% three months after augmentation (V2), 33.96% one year after augmentation (V3), and 37.96% three years after augmentation (V4). The most important finding of the present study is that
Fig. 5. Average volumes of grafted donor sites measured during the cone-beam computed tomography (CBCT) evaluations periods. V0: preoperative period; V1: postoperative first week; V2: postoperative third month before implant surgery; V3: postoperative first year; V4: postoperative third year; *: denotes statistically significant difference among volumes of grafted donor sites (P < 0.013).
Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004
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Figure 6. Average ( standard deviation) amount of the grafted iliac bone resorption. *: denotes the statistically significant difference between resorption volumes.
the resorption rates reduced significantly with time. The implants were placed three months after augmentation and loaded three months after the placement. Therefore, we may suggest that early implant placement and loading may reduce bone resorption rates over time in iliac grafting procedures. The mechanism associated with bone graft resorption is still not clearly understood [15]. In our study, we did not find any statistically significant relationship between resorption volume and gender, the presence of concurrent vestibuloplasty, and patient age. Johansson et al. suggested that a greater initial graft volume correlated with higher resorption rates [20]. In our study, we harvested tricortical large cortico-cancellous iliac block bone grafts. According to our results, we cannot agree with the suggestion reported by Johansson et al. [20] Higher resorption rates in large grafts might be associated with the increasing difficulties of ensuring primary closure which needs careful release of the soft tissue as reported by Dreiseidler et al. [22] In our study, despite the placement of large cortico-cancellous graft, no exposure of the graft was observed because of the passive closure of the mucosa at the recipient site. Dental implant placement and success pose challenges in the case of the severely resorbed maxilla. The reasons for multiple implant failures in grafted bone are important, and local and systemic factors may influence the implant survival rate [23]. Barone and Covani [15] reported the implant failure rate as 5.1% in severely resorbed maxillae grafted with anterior corticocancellous iliac crest. All implant failures occurred during the first six months after placement and prior to implant loading. There are still controversies regarding the time of the placement of the implants at the grafted area. Despite a one-stage protocol reducing the number of surgical procedures, most clinicians suggest performing a two-stage protocol [24–26]. The present study demonstrated the results of a two-stage approach. Three of 135 dental implants used for prosthodontic rehabilitations failed after loading (97.8% survival rate). Two of the failed implants were placed at the posterior maxilla and the third implant was placed at the anterior maxilla. There was no systemic disease history or smoking habit in the patients who suffered implant failure. Therefore, the failures may have been associated with the reduced bone volume at the surgical sites of the implants. The survival rate of the implants was found slightly higher than those reported by Barone and Covani [15] and Pereira et al. [14] and slightly lower than those reported by Sbordone et al. [21].
5. Conclusion The success rate of the iliac bone block grafts was found to be high. The volumetric resorption rates associated with the graft were favourable for the reconstruction of the atrophic maxilla and for permitting the insertion of dental implants three months following augmentation. The highest graft resorption was found in the third postoperative month. Placement and loading of the implants reduced the resorption rate slightly over time. Disclosure of interest The authors declare that they have no competing interest.
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Please cite this article in press as: Cansiz E, et al. Long-term evaluation of three-dimensional volumetric changes of augmented severely atrophic maxilla by anterior iliac crest bone grafting. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/ j.jormas.2019.11.004