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Survival rate of osseointegrated implants in atrophic maxillae grafted with calvarial bone: a retrospective study
Int. J. Oral Maxillofac. Surg. 2015; 44: 239–244 http://dx.doi.org/10.1016/j.ijom.2014.10.008, available online at http://www.sciencedirect.com
Clinical Paper Pre-Implant Surgery
Survival rate of osseointegrated implants in atrophic maxillae grafted with calvarial bone: a retrospective study
J. C. Quiles1, F. A. Souza2, A. P. F. Bassi2, I. R. Garcia Jr.2, M. T. Franc¸a3, P. S. P. Carvalho1,2 1
Sa˜o Leopoldo Mandic School of Dentistry and Research Center, Campinas, Brazil; 2 Department of Surgery and Integrated Clinic, Arac¸atuba Dental of School, Universidade Estadual Paulista Ju´lio de Mesquita Filho, Sa˜o Paulo, Brazil; 3Private Practice Clinic, Arac¸atuba, Brazil
J. C. Quiles, F. A. Souza, A. P. F. Bassi, I. R. Garcia Jr. , M. T. Franc¸a, P. S. P. Carvalho: Survival rate of osseointegrated implants in atrophic maxillae grafted with calvarial bone: a retrospective study. Int. J. Oral Maxillofac. Surg. 2015; 44: 239– 244. # 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. The aim of this study was to evaluate the clinical survival rate of osseointegrated implants placed in the atrophic maxilla that has been reconstructed by means of autogenous bone grafts harvested from a cranial calvarial site. Further, we sought to analyse the level of peri-implant bone after prosthetic rehabilitation and to determine subjective patient satisfaction with the treatment performed. This study conformed to the STROBE guidelines regarding retrospective studies. Twenty-five patients who had received osseointegrated implants with late loading in the reconstructed atrophic maxilla were included in the study. The survival rate and level of peri-implant bone loss were evaluated. A questionnaire related to the surgical and prosthetic procedures was completed. The observed implant survival rate was 92.35%. The mean bone loss recorded was 1.76 mm in the maxilla and 1.54 mm in the mandible. The results of the questionnaire indicated a high level of patient satisfaction, little surgical discomfort, and that the patients would recommend the procedure and would undergo the treatment again. From the results obtained, it is concluded that the cranial calvarial site is an excellent donor area; calvarial grafts provided stability and maintenance of bone volume over the course of up to 11 years.
The consequence of the absence of a tooth is continuous bone resorption. Depending on the period over which this occurs, it may become unfeasible to place implants in the edentulous region due to the absence of the minimum bone height and/or thickness required.1,2 The surgical procedure most often used for the reconstruction of these areas is bone grafting, for which materials 0901-5027/020239 + 06
of autogenous, homogeneous, heterogeneous, or synthetic origin may be applied. Material of autogenous origin is the only type that presents the biological property of osteogenicity. The scientific literature presents a wide variety of possible donor areas, both intraoral and extraoral. The latter include the cranial calvarium,3–5 fibula,6 iliac crest,7–9 rib,10,11 and tibia.12,13
Key words: bone graft; cranial calvarial; osseointegrated implants; implant survival; marginal bone loss; subjective evaluation. Accepted for publication 8 October 2014 Available online 4 November 2014
Among the possible extraoral donor areas, the most commonly used and studied is the iliac crest. This is characterized by corticomedullary bone with a predominance of the medullary portion, which has a good thickness. Its surgical advantages include better acceptance by the patient and a shorter surgical time, due to the possibility of simultaneously opening
# 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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the receptor and donor areas. However, it leads to a higher rate of complications and morbidity, greater need for analgesics, greater susceptibility to infection, longer hospitalization time, greater postsurgical remodelling of the bone graft, and a higher failure of implants placed in these areas when compared with the calvarial cranial donor site, and also results in an external scar.14 With the iliac crest graft, postsurgical discomfort in the donor area lasting months or even years has been reported, in addition to pain on walking.15 Another commonly used donor site is the cranial calvarium. This bone is of a membranous origin, formed of bones of the cortical and spongy types, with a predominance of the cortical portion. It presents rapid vascularization at the grafted site, which is a prerequisite for successful osteogenesis.3 There are many advantages to the choice of calvarial bone. This procedure presents a lower rate of complications and morbidity, a reduction in pain at the donor site, is less susceptible to infection, is subject to less resorption and postsurgical remodelling of the graft, involves a shorter hospitalization, and demonstrates higher success rates and better bone quality in comparison with the iliac crest graft; it also results in an imperceptible scar and does not affect respiration or walking.4,16 The follow-up of clinical cases submitted to reconstructive surgery of the atrophic maxilla and mandible has become important in terms of evaluating patient satisfaction and the effectiveness of the
procedure before undertaking the practice of extensive rehabilitations using bone grafts and implants. Within this context, the aim of the present study was to perform a retrospective evaluation of the success of implants placed in the atrophic maxilla reconstructed with autogenous bone obtained from the cranial calvarium, and to measure the patients’ personal satisfaction with their treatment from the initial surgical stage through to the conclusion of the rehabilitative stage.
Materials and methods
The STROBE guidelines (Strengthening the Reporting of Observational studies in Epidemiology) were followed for this retrospective study. The clinical records of 32 patients treated at the Continuing Education Nucleus (Nec-Odonto) post-graduate institution specializing in implant dentistry in Arac¸atuba, Brazil were retrieved from the database. All of these patients underwent reconstructive surgery by means of autogenous bone grafts harvested from the cranial calvarium with later placement of osseointegrated implants. Of these 32 patients, one could not be contacted at the address or using the telephone number provided in the clinical records, one patient was travelling in another country and had no return date, one patient was hospitalized, three patients did not respond to the telephone call or letter, and one patient had not yet completed the
Fig. 1. Flow diagram of patient selection for this study.
final prosthetic phase (Fig. 1). Hence the study included a total of 25 patients. Twenty of the patients were women and five were men, and they ranged in age from 43 to 75 years (mean 57 years). These patients underwent the surgical and rehabilitative procedures during the years 1999–2011. The inclusion criteria used were: (1) Patients who were partially or completely edentulous in the maxilla and/or mandible, who presented severe atrophy in height and/or thickness making it impossible to perform rehabilitation with dental implants, those with significant deficiencies in residual bone below the nasal cavity and maxillary sinus, and those with the absence of teeth due to agenesis; these patients had to have undergone reconstructive surgery with autogenous bone harvested from the calvarial cranial site. (2) Patients whose treatment was completed with an implantsupported denture that had been in place for at least 6 months. (3) Patient agreement and the provision of a signed term of free and informed consent. The exclusion criteria were the following: (1) Patients intellectually incapable of responding to the psychosocial evaluation questions about the rehabilitative treatment received. (2) Patients who did not complete the prosthetic rehabilitation. All patients evaluated underwent bone reconstruction surgery by means of autogenous bone grafts harvested from the cranial calvarium. The surgeries were performed in a hospital environment, under
Implants in maxillae grafted with calvarial bone general anaesthesia, with nasotracheal intubation, and all cases were indicated, planned, and carried out by the same multiprofessional team. All of the reconstructed maxillae were shown to be atrophied with a residual bone thickness of 1– 2 mm and a residual bone height of 10 mm. The dimensions of the residual maxillary bone were compatible with Cawood and Howell17 classification IV for the anterior maxilla and classification VI for the posterior maxilla. The indication was made when the patient required an increased thickness and/ or height of the ridge, and/or a unilateral or bilateral sinus lift. Panoramic radiographs and computed tomography examinations were used for planning. In the clinical– radiographic examination, the intraoral condition, state of conservation of the teeth, periodontal condition, presence of peri-apical lesions, and need for a provisional denture were evaluated; in addition, the patient’s psychological condition and acceptance of having the treatment performed were observed at this stage. At all times, the graft from the calvarium was harvested by a neurosurgeon, who obtained surgical access by dermoperiosteal incision in the lateral region of the head using the lateral corner of the orbit as reference. The area of graft collection in the calvarium was the parietal bone. After the use of a trephine bur to determine the external cortical thickness, the oral and maxillofacial surgeon performed the osteotomies necessary for reconstruction of the area to be grafted, followed by removal of the graft blocks by means of chisels and a hammer. After obtaining the graft, the surgical reconstruction procedure was performed. Access to the atrophic maxilla was gained by a mucoperiosteal incision in the alveolar crest, with relaxing incisions in the midline and posterior region on the right and left sides. After detachment and exposure of the tissues, an osteotomy was performed in the anterior wall of the maxillary sinus, and then the sinus membrane
was carefully detached. At all times, decorticalization was performed of the bone walls that were going to be constructed. After this, the bone blocks were modelled to the areas to be reconstructed, filling the maxillary sinus, or the maxillary sinuses, with particulated bone, in accordance with the initial indication and planning, and the bone blocks were fixed by means of cortical screws. As is the rule, each graft block was fixed with two cortical screws whenever possible. The goal of surgical reconstruction was to reconstruct the atrophic areas in which implants would later be placed, in accordance with the initial rehabilitation planning (Fig. 2). Temporary implants were placed for retaining a removable denture without buccal flanges, where appropriate. The implants were placed at 6 months after the reconstructive surgery when the graft was to increase bone thickness, or at 8 months after surgery in cases in which there was sinus grafting. The implant placement surgery was performed under local anaesthesia, and the number and distribution of the implants were determined by the prosthetic planning. All implants placed were of external hexagon type, regular Bra˚nemark standard platform of 4.1 mm, modified by dual acid etching surface (Conexa˜o Sistemas de Pro´tese, Sa˜o Paulo, Brazil), and ranged in length from 10.0 mm to 13.0 mm. The data relative to treatment, such as the date of each stage (reconstruction by means of graft, implant placement, and prosthetic completion), and data on graft complications and loss of implants were acquired from the clinical records of each patient. During the postoperative period, the patients were monitored by means of monthly visits. Panoramic radiographs were taken preoperatively, immediately postoperative, at 6–8 months after the reconstruction procedure (the stage before implant placement), after implant placement, after prosthetic rehabilitation, and at postsurgical follow-up after the bone
Fig. 2. Atrophic maxilla reconstructed with autogenous bone grafts harvested from the calvarium site (parietal bone).
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reconstruction period (condition in which the patients were found when they were invited to participate in this retrospective study). This study was approved by the committee on human research of the study institution. Clinical–radiographic evaluation
Evaluation of the success of implants was made by clinical–radiographic evaluation in accordance with the criteria for the evaluation of implant survival suggested by Chiapasco et al.18: the absence of persistent pain or dysesthesia, absence of peri-implant infection with suppuration, absence of mobility, and absence of continuous peri-implant radiolucency. To obtain the data on peri-implant bone loss, panoramic radiographs were digitized. The measurements were obtained by means of the program CDR DICOM for Windows (Schick Technologies, Long Island City, NY, USA) and performed by a single investigator. Implant length, previously known, was measured using the calibration tool of the program. Thereafter, bone loss measurements were taken at the union between the implant platform and the abutment up to the first bone– implant contact in the mesial and distal region of each implant (Fig. 3). Patients were divided into three groups by length of follow-up after the bone graft reconstruction. Group I comprised 16 subjects at 0–5 years post-surgical bone graft (13 maxilla only and three maxilla and mandible). Group II comprised five subjects at 6–10 years post-surgical bone graft (two maxilla only and three maxilla and mandible). Group III comprised four subjects at 11 years post-surgical bone graft (all maxilla only). Subjective evaluation of personal satisfaction
All patients included in this study provided free and informed consent. Sixteen patients participated in this part of the analysis. Nine patients did not respond to the questionnaire as they were unable to attend the appointment on the day and at the time set for reasons of work, health, travel, or distance from the place where they lived. A questionnaire was prepared with questions covering embarrassment, difficulties, and dissatisfactions, in addition to questions evaluating the patient’s perception of the surgical procedure as regards cost, information received before surgery was performed, satisfaction with the implants, and whether they would
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Quiles et al. implants, no new implants were placed. These implants were not placed, because their absence did not interfere with the end result of the prosthetic rehabilitation. The reason for the loss of these 15 implants was a lack of osseointegration, which was diagnosed by means of the mobility of the implants during the stage of re-opening. There was no infection at the site of implant loss, or suture dehiscence. The distribution of implants by dental arch and surgical follow-up in this retrospective study was as follows: group I (0– 5 years post-surgical bone graft), 116 implants (103 in the maxilla and 13 in the posterior mandible); group II (6–10 years post-surgical bone graft), 40 implants (31 in the maxilla and nine in the posterior mandible); group III (11 years post-surgical bone graft), 25 implants in the maxilla.
Fig. 3. Calibration and measurement made at the union between the implant platform and abutment up to the first bone–implant contact after calibrating the ruler.
recommend the procedure or would undergo the treatment again. With regard to prosthetic rehabilitation, questions were asked about aesthetics, phonetics, mastication, the comfort provided by the prosthetic rehabilitation, and the impact of treatment performed on their general health. The answers obtained were collected into four groups, as follows: group 1 – guidance, investment, and satisfaction with the professional and the work that was done; group 2 – surgical stage, complications, and pain; group 3 – would recommend the procedure to another person, or willing to undergo the treatment again; group 4 – restorative and aesthetic procedure, mastication, speech, sense of taste, and possible embarrassments.
Results
A total of 196 implants were placed; 15 implants were lost. From the survey of the clinical records, 181 implants were osseointegrated: 64 in the anterior maxilla, 95 in the posterior maxilla, and 22 in the posterior mandible. In the cases of all of the 15 implants that were lost, the loss occurred before the stage of prosthetic rehabilitation. After the definitive prosthetic rehabilitation, no implant was lost. For the 15 implants lost, nine new implants were reinserted in the same implantation sites 4 months later; these became osseointegrated, without any revision of the prosthetic rehabilitation planning being necessary. At the sites of the remaining six lost
Clinical–radiographic evaluation
The overall survival rate of the implants placed was 92.35%. The survival rate of implants after prosthetic rehabilitation was 92.75% for the anterior maxilla, 91.34% for the posterior maxilla, and 95.66% for the posterior mandible (Fig. 4). In general the mean bone loss recorded was 1.76 mm in the maxilla and 1.54 mm in the mandible. The mean peri-implant bone loss in the maxilla ranged from 1.38 mm to 2.10 mm (Fig. 5) depending on the period of follow-up and site analysed. In the mandible, peri-implant bone loss ranged from 1 mm to 2.1 mm (Fig. 6) depending on the period of follow-up and site analysed. Subjective evaluation of personal satisfaction
Nine patients in group I, four in group II, and three in group III returned for subjective evaluation of personal satisfaction. The rates of satisfaction and dissatisfaction and the profile of patients according to the questionnaire are shown in Fig. 7. Discussion
Fig. 4. Distribution of the percentage survival of implants according to the region grafted.
A comparison of the success rate obtained in this study to those reported in the few articles on retrospective studies of grafts obtained from the calvarium, showed similar results. In the study by Donovan et al., a success rate of 91.4% was reported for implants placed in 24 patients who had areas reconstructed with bone harvested from the calvarium.19 Mertens et al. showed a success rate of 95.7% for
Implants in maxillae grafted with calvarial bone
Fig. 5. Mean values of peri-implant bone loss in the maxilla according to the time period and site analysed.
implants placed in the maxilla (n = 15) and mandible (n = 4) reconstructed with bone obtained from the cranium.20 The loss of a total 15 implants (7.65%) was observed in this study. Five were lost in the anterior maxilla (7.25%) and nine in the posterior maxilla (8.66%). Basically, these implants were inserted in grafted
bone, since the primitive bone thickness was about 1 mm in the vestibulo-palatine direction in the anterior region of the maxilla and maxillary sinus, with the floor at the level of the alveolar crest. In two patients, simultaneous loss occurred of implants inserted in the anterior and posterior maxilla. The loss of only one
Fig. 6. Mean values of peri-implant bone loss in the mandible according to the time period and site analysed.
Fig. 7. The patients’ perception of the surgical (graft and implants) and prosthetic procedures involved in rehabilitation.
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implant in the posterior mandible was observed (4.34%). At the sites where the implants were lost, new implants were placed without further intercurrence, enabling the prosthetic rehabilitation of the patients to proceed as initially planned. Another analysis done in this study was the measurement of bone loss in millimetres. Measurements were taken from the abutment–implant union up to the first mesial and distal bone contact. The mean bone loss in millimetres in the first 5 years was 1.74 mm in the maxilla and 1.08 mm in the mandible. There is a consensus that bone loss in the first year of function ranges from 0.5 to 3 mm.21 However, the mean marginal bone losses obtained in this study were lower than those reported in other studies, such as that conducted by Ko¨ndell et al., 10 in which implants placed in areas reconstructed with grafts obtained from the rib had a mean marginal bone loss of 2.15 mm after 1 year. Becktor et al.22 observed a mean bone loss of 3.3 mm after a follow-up of 5–6 years in implants placed in areas reconstructed with iliac crest grafts. Nystro¨m et al., in a study with 10 years of follow-up, found a mean bone loss associated with implants placed in an area reconstructed with a graft obtained from the iliac crest of 2.23 mm in women and 2.60 mm in men.15 According to reports in the literature, the most common complication of grafts obtained from the calvarial site is postoperative pain. However, this is minimal or non-existent, and when it persists, relief is obtained by means of analgesia.23,24 A personal satisfaction questionnaire was used in this study, and 68.75% of the patients reported that they had not experienced any pain symptoms. However, 18.75% of the patients reported the presence of pain in the postoperative period, in which discomfort lasted on average 1 week. Similar results were found in another study.25 No problem with the lesion or neurological compromise was mentioned. Gutta and Waite16 related not having noted any neurosurgical disturbance in their study of patients who underwent surgery for reconstruction by means of a graft obtained from the cranial cap. Similar results were described by Orsini et al.,3 who reported the absence of laceration of the dura mater, bleeding or infection at the donor site, neurological injury, or prolonged postoperative pain. When asked whether they would be fully prepared to undergo the treatment again, or to recommend the treatment to someone else, the study patients were
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unanimous in their affirmation of agreement, as also observed in another study.20 From the results of this study, it is possible to confirm that the cranial cap is a suitable donor source of autogenous bone tissue for use in the reconstruction of the atrophic maxilla and allows the placement of implants with predictable success. In addition, this donor area presents minimal morbidity and patients undergoing these reconstructive procedures are highly satisfied with the results.
6.
7.
8.
Funding
None. 9.
Competing interests
None declared.
10.
Ethical approval
This study was submitted to the Committee on Human Research of Sa˜o Leopoldo Mandic School of Dentistry and Research Centre and received approval (protocol number 2011/0009).
11.
12.
References 1. Arau´jo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 2005;32:212–8. 2. Van Der Weijden F, Dell’Acqua F, Slot DE. Alveolar bone dimensional changes of post-extraction sockets in humans: a systematic review. J Clin Periodontol 2009;36:1048–58. 3. Orsini G, Bianchi AE, Vinci R, Piatelli A. Histologic evaluation of autogenous calvarial bone in maxillary onlay bone grafts: a report of 2 cases. Int J Oral Maxillofac Implants 2003;18:594–8. 4. Carvalho PS, Bassi AP, Garcia Jr IR, Franc¸a MT, Ponzoni D. Enxerto de calota craniana para reconstruc¸a˜o de processo alveolar de maxila atro´fica. Te´cnica de obtenc¸a˜o e dificuldades transoperato´rias. Implant News 2006;3:572–7. 5. Gutta R, Waite PD. Cranial bone grafting and simultaneous implants: a submental
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technique to reconstruct the atrophic mandible. J Oral Maxillofac Surg 2008;46:477–9. Gbara D, Darwich K, Li L, Schmelzle R, Blake F. Long-term results of jaw reconstruction with microsurgical fibula grafts and dental implants. J Oral Maxillofac Surg 2007;65:1005–9. Adell R, Lekholm U, Gro¨ndahl K, Bra˚nemark PI, Lindstro¨n J, Jacobsson M. Reconstruction of severely resorbed edentulous maxillae using osseointegrated fixtures in immediate autogenous bone grafts. Int J Oral Maxillofac Implants 1990;5:233–46. Stellingsma C, Vissink A, Meijer HJ, Kuiper C, Raghoebar GM. Implantology and the severely resorbed edentulous mandible. Crit Rev Oral Biol Med 2004;15:240–8. Barone A, Covani U. Maxillary alveolar ridge reconstruction with nonvascularized autogenous block bone: clinical results. J Oral Maxillofac Surg 2007;65:2039–46. Ko¨ndell PA, Nordenram A, Moberg LE, Eliasson S, Nyberg B. Reconstruction of the resorbed edentulous maxilla using autogenous rib grafts and osseointegrated implants. Clin Oral Implants Res 1996;7: 286–90. Li Z, Zhao Y, Yao S, Zhao J, Yu S, Zhang W. Immediate reconstruction of mandibular defects: a retrospective report of 242 cases. J Oral Maxillofac Surg 2007;65:883–90. Breine U, Bra˚nemark PI. Reconstruction of alveolar jaw bone. An experimental and clinical study of immediate and preformed autologous bone grafts in combination with osseointegrated implants. Scand J Plast Reconstr Surg 1980;14:23–48. Gerressen M, Prescher A, Riediger D, van der Ven D, Ghassemi A. Tibial versus iliac bone grafts: a comparative examination in 15 freshly preserved adult cadavers. Clin Oral Implants Res 2008;19:1270–5. Crespi R, Vinci R, Cappare` P, Gherlone E, Romanos GE. Calvarial versus iliac crest for autologous bone graft materials for a sinus lift procedure: a histomorphometric study. Int J Oral Maxillofac Implants 2007;22: 427–32. Nystro¨m E, Nilson H, Gunne J, Lundgren S. A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla. Int J Oral Maxillofac Surg 2009;38:111–6. Gutta R, Waite PD. Outcomes of calvarial bone grafting for alveolar ridge reconstruction. Int J Oral Maxillofac Implants 2009; 24:131–6.
17. Cawood JL, Howell RA. A classification of the edentulous jaws. Int J Oral Maxillofac Surg 1988;17:232–6. 18. Chiapasco M, Romeo E, Coggiola A, Brusati R. Long-term outcome of dental implants placed in revascularized fibula free flaps used for the reconstruction of maxillo-mandibular defects due to extreme atrophy. Clin Oral Implants Res 2011;22:83–91. 19. Donovan MG, Dickerson NC, Hanson LJ, Gustafson RB. Maxillary and mandibular reconstruction using calvarial bone grafts and Bra˚nemark implants: a preliminary report. J Oral Maxillofac Surg 1994;52: 588–94. 20. Mertens C, Steveling HG, Seeberger R, Hoffmann J, Freier K. Reconstruction of severely atrophied alveolar ridges with calvarial onlay bone grafts and dental implants. Clin Implant Dent Relat Res 2013;15: 673–83. 21. Misch CE, Dietsh F. Autogenous bone grafts for endosteal implants – indications and failures. Int J Oral Implantol 1991;8:13–20. 22. Becktor JP, Isaksson S, Sennerby L. Endosseous implants and bone augmentation in the partially dentate maxilla: an analysis of 17 patients with a follow-up of 29 to 101 months. Int J Oral Maxillofac Implants 2007;22:603–8. 23. Harsha BC, Turvey TA, Powers SK. Use of autogenous cranial bone grafts in maxillofacial surgery: a preliminary report. J Oral Maxillofac Surg 1986;44:11–5. 24. Sammartino G, Marenzi G, Colella G, Califano L, Grivetto F, Mortellaro C. Autogenous calvarial bone graft harvest: intraoperational complications. J Craniofac Surg 2005;16:312–9. 25. Pastori CM, Marzola C, Toledo-Neto JL, Vago TM, Toledo-Filho JL, Capelari MM. Enxerto de calota craniana. Revista da literatura e apresentac¸a˜o de caso clı´nico ciru´rgico. Rev Odontol 2007;7:790–807.
Address: Francisley A´vila Souza Department of Surgery and Integrated Clinic Arac¸atuba Dental of School Universidade Estadual Paulista Ju´lio de Mesquita Filho Rua Jose´ Bonifacio 1193 Arac¸atuba Sa˜o Paulo Brazil Tel: +55 18 36362898 E-mail: [email protected]
Clinical Paper Pre-Implant Surgery
Survival rate of osseointegrated implants in atrophic maxillae grafted with calvarial bone: a retrospective study
J. C. Quiles1, F. A. Souza2, A. P. F. Bassi2, I. R. Garcia Jr.2, M. T. Franc¸a3, P. S. P. Carvalho1,2 1
Sa˜o Leopoldo Mandic School of Dentistry and Research Center, Campinas, Brazil; 2 Department of Surgery and Integrated Clinic, Arac¸atuba Dental of School, Universidade Estadual Paulista Ju´lio de Mesquita Filho, Sa˜o Paulo, Brazil; 3Private Practice Clinic, Arac¸atuba, Brazil
J. C. Quiles, F. A. Souza, A. P. F. Bassi, I. R. Garcia Jr. , M. T. Franc¸a, P. S. P. Carvalho: Survival rate of osseointegrated implants in atrophic maxillae grafted with calvarial bone: a retrospective study. Int. J. Oral Maxillofac. Surg. 2015; 44: 239– 244. # 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. The aim of this study was to evaluate the clinical survival rate of osseointegrated implants placed in the atrophic maxilla that has been reconstructed by means of autogenous bone grafts harvested from a cranial calvarial site. Further, we sought to analyse the level of peri-implant bone after prosthetic rehabilitation and to determine subjective patient satisfaction with the treatment performed. This study conformed to the STROBE guidelines regarding retrospective studies. Twenty-five patients who had received osseointegrated implants with late loading in the reconstructed atrophic maxilla were included in the study. The survival rate and level of peri-implant bone loss were evaluated. A questionnaire related to the surgical and prosthetic procedures was completed. The observed implant survival rate was 92.35%. The mean bone loss recorded was 1.76 mm in the maxilla and 1.54 mm in the mandible. The results of the questionnaire indicated a high level of patient satisfaction, little surgical discomfort, and that the patients would recommend the procedure and would undergo the treatment again. From the results obtained, it is concluded that the cranial calvarial site is an excellent donor area; calvarial grafts provided stability and maintenance of bone volume over the course of up to 11 years.
The consequence of the absence of a tooth is continuous bone resorption. Depending on the period over which this occurs, it may become unfeasible to place implants in the edentulous region due to the absence of the minimum bone height and/or thickness required.1,2 The surgical procedure most often used for the reconstruction of these areas is bone grafting, for which materials 0901-5027/020239 + 06
of autogenous, homogeneous, heterogeneous, or synthetic origin may be applied. Material of autogenous origin is the only type that presents the biological property of osteogenicity. The scientific literature presents a wide variety of possible donor areas, both intraoral and extraoral. The latter include the cranial calvarium,3–5 fibula,6 iliac crest,7–9 rib,10,11 and tibia.12,13
Key words: bone graft; cranial calvarial; osseointegrated implants; implant survival; marginal bone loss; subjective evaluation. Accepted for publication 8 October 2014 Available online 4 November 2014
Among the possible extraoral donor areas, the most commonly used and studied is the iliac crest. This is characterized by corticomedullary bone with a predominance of the medullary portion, which has a good thickness. Its surgical advantages include better acceptance by the patient and a shorter surgical time, due to the possibility of simultaneously opening
# 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
240
Quiles et al.
the receptor and donor areas. However, it leads to a higher rate of complications and morbidity, greater need for analgesics, greater susceptibility to infection, longer hospitalization time, greater postsurgical remodelling of the bone graft, and a higher failure of implants placed in these areas when compared with the calvarial cranial donor site, and also results in an external scar.14 With the iliac crest graft, postsurgical discomfort in the donor area lasting months or even years has been reported, in addition to pain on walking.15 Another commonly used donor site is the cranial calvarium. This bone is of a membranous origin, formed of bones of the cortical and spongy types, with a predominance of the cortical portion. It presents rapid vascularization at the grafted site, which is a prerequisite for successful osteogenesis.3 There are many advantages to the choice of calvarial bone. This procedure presents a lower rate of complications and morbidity, a reduction in pain at the donor site, is less susceptible to infection, is subject to less resorption and postsurgical remodelling of the graft, involves a shorter hospitalization, and demonstrates higher success rates and better bone quality in comparison with the iliac crest graft; it also results in an imperceptible scar and does not affect respiration or walking.4,16 The follow-up of clinical cases submitted to reconstructive surgery of the atrophic maxilla and mandible has become important in terms of evaluating patient satisfaction and the effectiveness of the
procedure before undertaking the practice of extensive rehabilitations using bone grafts and implants. Within this context, the aim of the present study was to perform a retrospective evaluation of the success of implants placed in the atrophic maxilla reconstructed with autogenous bone obtained from the cranial calvarium, and to measure the patients’ personal satisfaction with their treatment from the initial surgical stage through to the conclusion of the rehabilitative stage.
Materials and methods
The STROBE guidelines (Strengthening the Reporting of Observational studies in Epidemiology) were followed for this retrospective study. The clinical records of 32 patients treated at the Continuing Education Nucleus (Nec-Odonto) post-graduate institution specializing in implant dentistry in Arac¸atuba, Brazil were retrieved from the database. All of these patients underwent reconstructive surgery by means of autogenous bone grafts harvested from the cranial calvarium with later placement of osseointegrated implants. Of these 32 patients, one could not be contacted at the address or using the telephone number provided in the clinical records, one patient was travelling in another country and had no return date, one patient was hospitalized, three patients did not respond to the telephone call or letter, and one patient had not yet completed the
Fig. 1. Flow diagram of patient selection for this study.
final prosthetic phase (Fig. 1). Hence the study included a total of 25 patients. Twenty of the patients were women and five were men, and they ranged in age from 43 to 75 years (mean 57 years). These patients underwent the surgical and rehabilitative procedures during the years 1999–2011. The inclusion criteria used were: (1) Patients who were partially or completely edentulous in the maxilla and/or mandible, who presented severe atrophy in height and/or thickness making it impossible to perform rehabilitation with dental implants, those with significant deficiencies in residual bone below the nasal cavity and maxillary sinus, and those with the absence of teeth due to agenesis; these patients had to have undergone reconstructive surgery with autogenous bone harvested from the calvarial cranial site. (2) Patients whose treatment was completed with an implantsupported denture that had been in place for at least 6 months. (3) Patient agreement and the provision of a signed term of free and informed consent. The exclusion criteria were the following: (1) Patients intellectually incapable of responding to the psychosocial evaluation questions about the rehabilitative treatment received. (2) Patients who did not complete the prosthetic rehabilitation. All patients evaluated underwent bone reconstruction surgery by means of autogenous bone grafts harvested from the cranial calvarium. The surgeries were performed in a hospital environment, under
Implants in maxillae grafted with calvarial bone general anaesthesia, with nasotracheal intubation, and all cases were indicated, planned, and carried out by the same multiprofessional team. All of the reconstructed maxillae were shown to be atrophied with a residual bone thickness of 1– 2 mm and a residual bone height of 10 mm. The dimensions of the residual maxillary bone were compatible with Cawood and Howell17 classification IV for the anterior maxilla and classification VI for the posterior maxilla. The indication was made when the patient required an increased thickness and/ or height of the ridge, and/or a unilateral or bilateral sinus lift. Panoramic radiographs and computed tomography examinations were used for planning. In the clinical– radiographic examination, the intraoral condition, state of conservation of the teeth, periodontal condition, presence of peri-apical lesions, and need for a provisional denture were evaluated; in addition, the patient’s psychological condition and acceptance of having the treatment performed were observed at this stage. At all times, the graft from the calvarium was harvested by a neurosurgeon, who obtained surgical access by dermoperiosteal incision in the lateral region of the head using the lateral corner of the orbit as reference. The area of graft collection in the calvarium was the parietal bone. After the use of a trephine bur to determine the external cortical thickness, the oral and maxillofacial surgeon performed the osteotomies necessary for reconstruction of the area to be grafted, followed by removal of the graft blocks by means of chisels and a hammer. After obtaining the graft, the surgical reconstruction procedure was performed. Access to the atrophic maxilla was gained by a mucoperiosteal incision in the alveolar crest, with relaxing incisions in the midline and posterior region on the right and left sides. After detachment and exposure of the tissues, an osteotomy was performed in the anterior wall of the maxillary sinus, and then the sinus membrane
was carefully detached. At all times, decorticalization was performed of the bone walls that were going to be constructed. After this, the bone blocks were modelled to the areas to be reconstructed, filling the maxillary sinus, or the maxillary sinuses, with particulated bone, in accordance with the initial indication and planning, and the bone blocks were fixed by means of cortical screws. As is the rule, each graft block was fixed with two cortical screws whenever possible. The goal of surgical reconstruction was to reconstruct the atrophic areas in which implants would later be placed, in accordance with the initial rehabilitation planning (Fig. 2). Temporary implants were placed for retaining a removable denture without buccal flanges, where appropriate. The implants were placed at 6 months after the reconstructive surgery when the graft was to increase bone thickness, or at 8 months after surgery in cases in which there was sinus grafting. The implant placement surgery was performed under local anaesthesia, and the number and distribution of the implants were determined by the prosthetic planning. All implants placed were of external hexagon type, regular Bra˚nemark standard platform of 4.1 mm, modified by dual acid etching surface (Conexa˜o Sistemas de Pro´tese, Sa˜o Paulo, Brazil), and ranged in length from 10.0 mm to 13.0 mm. The data relative to treatment, such as the date of each stage (reconstruction by means of graft, implant placement, and prosthetic completion), and data on graft complications and loss of implants were acquired from the clinical records of each patient. During the postoperative period, the patients were monitored by means of monthly visits. Panoramic radiographs were taken preoperatively, immediately postoperative, at 6–8 months after the reconstruction procedure (the stage before implant placement), after implant placement, after prosthetic rehabilitation, and at postsurgical follow-up after the bone
Fig. 2. Atrophic maxilla reconstructed with autogenous bone grafts harvested from the calvarium site (parietal bone).
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reconstruction period (condition in which the patients were found when they were invited to participate in this retrospective study). This study was approved by the committee on human research of the study institution. Clinical–radiographic evaluation
Evaluation of the success of implants was made by clinical–radiographic evaluation in accordance with the criteria for the evaluation of implant survival suggested by Chiapasco et al.18: the absence of persistent pain or dysesthesia, absence of peri-implant infection with suppuration, absence of mobility, and absence of continuous peri-implant radiolucency. To obtain the data on peri-implant bone loss, panoramic radiographs were digitized. The measurements were obtained by means of the program CDR DICOM for Windows (Schick Technologies, Long Island City, NY, USA) and performed by a single investigator. Implant length, previously known, was measured using the calibration tool of the program. Thereafter, bone loss measurements were taken at the union between the implant platform and the abutment up to the first bone– implant contact in the mesial and distal region of each implant (Fig. 3). Patients were divided into three groups by length of follow-up after the bone graft reconstruction. Group I comprised 16 subjects at 0–5 years post-surgical bone graft (13 maxilla only and three maxilla and mandible). Group II comprised five subjects at 6–10 years post-surgical bone graft (two maxilla only and three maxilla and mandible). Group III comprised four subjects at 11 years post-surgical bone graft (all maxilla only). Subjective evaluation of personal satisfaction
All patients included in this study provided free and informed consent. Sixteen patients participated in this part of the analysis. Nine patients did not respond to the questionnaire as they were unable to attend the appointment on the day and at the time set for reasons of work, health, travel, or distance from the place where they lived. A questionnaire was prepared with questions covering embarrassment, difficulties, and dissatisfactions, in addition to questions evaluating the patient’s perception of the surgical procedure as regards cost, information received before surgery was performed, satisfaction with the implants, and whether they would
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Quiles et al. implants, no new implants were placed. These implants were not placed, because their absence did not interfere with the end result of the prosthetic rehabilitation. The reason for the loss of these 15 implants was a lack of osseointegration, which was diagnosed by means of the mobility of the implants during the stage of re-opening. There was no infection at the site of implant loss, or suture dehiscence. The distribution of implants by dental arch and surgical follow-up in this retrospective study was as follows: group I (0– 5 years post-surgical bone graft), 116 implants (103 in the maxilla and 13 in the posterior mandible); group II (6–10 years post-surgical bone graft), 40 implants (31 in the maxilla and nine in the posterior mandible); group III (11 years post-surgical bone graft), 25 implants in the maxilla.
Fig. 3. Calibration and measurement made at the union between the implant platform and abutment up to the first bone–implant contact after calibrating the ruler.
recommend the procedure or would undergo the treatment again. With regard to prosthetic rehabilitation, questions were asked about aesthetics, phonetics, mastication, the comfort provided by the prosthetic rehabilitation, and the impact of treatment performed on their general health. The answers obtained were collected into four groups, as follows: group 1 – guidance, investment, and satisfaction with the professional and the work that was done; group 2 – surgical stage, complications, and pain; group 3 – would recommend the procedure to another person, or willing to undergo the treatment again; group 4 – restorative and aesthetic procedure, mastication, speech, sense of taste, and possible embarrassments.
Results
A total of 196 implants were placed; 15 implants were lost. From the survey of the clinical records, 181 implants were osseointegrated: 64 in the anterior maxilla, 95 in the posterior maxilla, and 22 in the posterior mandible. In the cases of all of the 15 implants that were lost, the loss occurred before the stage of prosthetic rehabilitation. After the definitive prosthetic rehabilitation, no implant was lost. For the 15 implants lost, nine new implants were reinserted in the same implantation sites 4 months later; these became osseointegrated, without any revision of the prosthetic rehabilitation planning being necessary. At the sites of the remaining six lost
Clinical–radiographic evaluation
The overall survival rate of the implants placed was 92.35%. The survival rate of implants after prosthetic rehabilitation was 92.75% for the anterior maxilla, 91.34% for the posterior maxilla, and 95.66% for the posterior mandible (Fig. 4). In general the mean bone loss recorded was 1.76 mm in the maxilla and 1.54 mm in the mandible. The mean peri-implant bone loss in the maxilla ranged from 1.38 mm to 2.10 mm (Fig. 5) depending on the period of follow-up and site analysed. In the mandible, peri-implant bone loss ranged from 1 mm to 2.1 mm (Fig. 6) depending on the period of follow-up and site analysed. Subjective evaluation of personal satisfaction
Nine patients in group I, four in group II, and three in group III returned for subjective evaluation of personal satisfaction. The rates of satisfaction and dissatisfaction and the profile of patients according to the questionnaire are shown in Fig. 7. Discussion
Fig. 4. Distribution of the percentage survival of implants according to the region grafted.
A comparison of the success rate obtained in this study to those reported in the few articles on retrospective studies of grafts obtained from the calvarium, showed similar results. In the study by Donovan et al., a success rate of 91.4% was reported for implants placed in 24 patients who had areas reconstructed with bone harvested from the calvarium.19 Mertens et al. showed a success rate of 95.7% for
Implants in maxillae grafted with calvarial bone
Fig. 5. Mean values of peri-implant bone loss in the maxilla according to the time period and site analysed.
implants placed in the maxilla (n = 15) and mandible (n = 4) reconstructed with bone obtained from the cranium.20 The loss of a total 15 implants (7.65%) was observed in this study. Five were lost in the anterior maxilla (7.25%) and nine in the posterior maxilla (8.66%). Basically, these implants were inserted in grafted
bone, since the primitive bone thickness was about 1 mm in the vestibulo-palatine direction in the anterior region of the maxilla and maxillary sinus, with the floor at the level of the alveolar crest. In two patients, simultaneous loss occurred of implants inserted in the anterior and posterior maxilla. The loss of only one
Fig. 6. Mean values of peri-implant bone loss in the mandible according to the time period and site analysed.
Fig. 7. The patients’ perception of the surgical (graft and implants) and prosthetic procedures involved in rehabilitation.
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implant in the posterior mandible was observed (4.34%). At the sites where the implants were lost, new implants were placed without further intercurrence, enabling the prosthetic rehabilitation of the patients to proceed as initially planned. Another analysis done in this study was the measurement of bone loss in millimetres. Measurements were taken from the abutment–implant union up to the first mesial and distal bone contact. The mean bone loss in millimetres in the first 5 years was 1.74 mm in the maxilla and 1.08 mm in the mandible. There is a consensus that bone loss in the first year of function ranges from 0.5 to 3 mm.21 However, the mean marginal bone losses obtained in this study were lower than those reported in other studies, such as that conducted by Ko¨ndell et al., 10 in which implants placed in areas reconstructed with grafts obtained from the rib had a mean marginal bone loss of 2.15 mm after 1 year. Becktor et al.22 observed a mean bone loss of 3.3 mm after a follow-up of 5–6 years in implants placed in areas reconstructed with iliac crest grafts. Nystro¨m et al., in a study with 10 years of follow-up, found a mean bone loss associated with implants placed in an area reconstructed with a graft obtained from the iliac crest of 2.23 mm in women and 2.60 mm in men.15 According to reports in the literature, the most common complication of grafts obtained from the calvarial site is postoperative pain. However, this is minimal or non-existent, and when it persists, relief is obtained by means of analgesia.23,24 A personal satisfaction questionnaire was used in this study, and 68.75% of the patients reported that they had not experienced any pain symptoms. However, 18.75% of the patients reported the presence of pain in the postoperative period, in which discomfort lasted on average 1 week. Similar results were found in another study.25 No problem with the lesion or neurological compromise was mentioned. Gutta and Waite16 related not having noted any neurosurgical disturbance in their study of patients who underwent surgery for reconstruction by means of a graft obtained from the cranial cap. Similar results were described by Orsini et al.,3 who reported the absence of laceration of the dura mater, bleeding or infection at the donor site, neurological injury, or prolonged postoperative pain. When asked whether they would be fully prepared to undergo the treatment again, or to recommend the treatment to someone else, the study patients were
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unanimous in their affirmation of agreement, as also observed in another study.20 From the results of this study, it is possible to confirm that the cranial cap is a suitable donor source of autogenous bone tissue for use in the reconstruction of the atrophic maxilla and allows the placement of implants with predictable success. In addition, this donor area presents minimal morbidity and patients undergoing these reconstructive procedures are highly satisfied with the results.
6.
7.
8.
Funding
None. 9.
Competing interests
None declared.
10.
Ethical approval
This study was submitted to the Committee on Human Research of Sa˜o Leopoldo Mandic School of Dentistry and Research Centre and received approval (protocol number 2011/0009).
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12.
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Address: Francisley A´vila Souza Department of Surgery and Integrated Clinic Arac¸atuba Dental of School Universidade Estadual Paulista Ju´lio de Mesquita Filho Rua Jose´ Bonifacio 1193 Arac¸atuba Sa˜o Paulo Brazil Tel: +55 18 36362898 E-mail: [email protected]