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A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla
Int. J. Oral Maxillofac. Surg. 2009; 38: 111–116 doi:10.1016/j.ijom.2008.10.008, available online at http://www.sciencedirect.com
Leading Clinical Paper Pre-Implant Surgery
A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla
E. Nystro¨m1, H. Nilson2, J. Gunne2, S. Lundgren1 1 Department of Oral Maxillofacial Surgery, Umea˚ University, Umea˚, Sweden; 2 Department of Prosthetic Dentistry, Umea˚ University, Umea˚, Sweden
E. Nystro¨m, H. Nilson, J. Gunne, S. Lundgren: A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla. Int. J. Oral Maxillofac. Surg. 2009; 38: 111–116. # 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Treatment of the atrophic edentulous maxilla is challenging especially when bone graft procedures are necessary. In this study an onlay bone graft, a saddle or veneer, with or without maxillary sinus floor inlay graft, harvested from the anterior iliac crest, in combination with implants was used in the reconstruction of patients with extreme atrophy in their maxillae. The aim was to investigate treatment outcome, and the impact of gender and smoking, in 44 patients in a prospective, long-term, follow-up study concerning implant survival rate and marginal bone loss adjacent to the surfaces of the implant. Mean follow-up time was 11 years. Of 334 inserted Bra˚nemark implants, with machined surface, 27 failed. Estimated implant survival rate was 90%. Marginal bone loss was 1.8 mm 1 year after implant surgery; 2.3 mm after 5 years; and 2.4 mm after 10 years. There was a significant difference between genders in implant survival. Marginal bone loss differed significantly between smokers and non-smokers up to the 5-year examination and between genders after the 4-year examination. The onlay bone graft, with or without a maxillary inlay graft, results in high implant survival rate, good oral function and stabilised marginal bone. All patients are still wearing their original fixed bridges.
In the atrophic edentulous maxilla, grafting procedures in combination with endosteal implants are necessary1,5,6,13,16,17,24,35. The final physiological resorption differs between patients, so different reconstructive techniques should be used, for example, in the thin alveolar process a saddle or veneer onlay graft can be chosen20, while if there are reversed intermaxillary relations or an increased vertical distance between the maxilla and mandible, an interposi0901-5027/020111 + 06 $30.00/0
tional bone graft and Le Fort I osteotomy is an alternative25. One requirement for successful treatment with endosteal implants is a sufficient amount of jaw bone. In patients with advanced resorption of the maxilla this bone is not available, therefore augmenting procedures to reconstruct the alveolar crest to increase the vertical and horizontal dimensions are necessary.
Keywords: bone grafting; autogenous bone; iliac crest; maxilla; implants; marginal bone level. Accepted for publication 28 October 2008 Available online 28 November 2008
The aim of reconstruction with bone grafts and implants is to restore facial morphology. The condition of the alveolar crest determines the choice of surgical technique to optimize function and appearance for the patient. The anterior iliac crest is a common donor site, especially when both cortical and cancellous bone are required. The medial table has a thin cortical plate compared with the superior or lateral borders of the iliac
# 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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crest. The area of the lateral iliac crest, where the medial gluteus muscle inserts, known as the tubercle, contains cortical bone with a high density and thickness. This area is preferable when large amounts of cortical bone are needed. The disadvantage of harvesting bone from the superior or lateral border of the iliac crests is that interference with the insertion of the gluteus muscles may cause gait disturbance10. The aims of this study were to evaluate the implant survival rate and marginal bone level after long-term follow-up and to study the impact of smoking and gender on these aspects.
Material and methods
This study comprised 44 consecutive edentate patients with maxillary atrophy, 15 men and 29 women. The patients were referred to the Department of Oral and Maxillofacial Surgery, Umea˚ University Hospital, for reconstruction of the maxillary alveolar ridge with bone grafts and implants. The mean age of the patients was 58 years (range 45–68 years). This group of patients was followed annually with a mean follow-up time of 11 years (range 9– 14 years) after the implant surgery. The patients in this study suffered from severe maxillary atrophy verified by clinical and tomographic examination. Most patients had sufficient bone height, but not sufficient width in the maxilla for implant treatment; class IV according to CAWOOD and HOWELL8. Some patients also had inadequate vertical height, more often seen in the anterior maxilla; class V according to CAWOOD and HOWELL8. Of the 44 patients, 24 underwent reconstruction in the anterior and posterior maxilla with an onlay bone graft; a veneer graft in the posterior maxilla and a veneer or saddle graft in the anterior maxilla. The remaining 20 patients had reconstruction with an onlay bone graft in the anterior maxilla and an inlay bone graft in the maxillary sinus floor bilaterally. Vertical augmentation of the nasal floor was performed with an onlay bone graft in 40 of the 44 patients. The 29 female patients received 223 implants and the 15 men received 111 implants. Twenty-seven patients were non-smokers and 5 patients had previously smoked but had stopped smoking before surgery; 12 patients were active smokers. In the smoking group of 12 patients 89 implants were inserted and in the nonsmoking group of 32 patients received 245 implants.
The patients had been edentate for a long time: 32 patients for more than 25 years (25–48 years), 4 patients for 10–25 years, and 7 patients for up to 10 years. Edentate duration was not reported for one patient. Of 44 patients, 22 were dentate or supported with an implant-supported fixed bridge in the mandible and 21 patients had an anterior dentition with or without removable prostheses. Only one patient in the study was edentate.
Reconstructive surgery
Surgery was performed under general anaesthesia with oral endotracheal intubation. A local anaesthetic with a vasoconstrictor was used for haemostasis. Bensylpenicillin, 3 g, were administered at the start of the operation. The iliac crest was chosen as the donor site. A corticocancellous block was harvested from the superolateral border of the iliac crest. The bone grafts were stored in blood-soaked gauze. The wound was closed in layers; the closure of the first layer, the fascia lata, was carefully readapted to avoid marrow bone bleeding into surrounding soft tissue. An activated vacuum drainage was positioned between the fascia lata and the muscles and kept in place until bleeding stopped, usually on the second postoperative day. The skin was closed with continuous intracutaneous sutures using resorbable material. Intraorally, a mucoperiosteal flap, labially directed through a midcrestal incision, was raised to expose the lateral wall of the sinus, nasal aperture and the anterior maxillary alveolar crest. The surgical bone-grafting procedure, preparation of the sinuses, and elevation of the sinus and nasal mucosa have been described previously20. The bone grafts were placed in the sinuses as well as on the anterior nasal floor and as veneer or saddle grafts on the alveolar ridge. The cortiococancellous bone blocks were adjusted and placed on the alveolar process and rigidly fixed with titanium screws (2 mm diameter). Each bone block was rigidly fixed with 2–3 screws engaging the total residual alveolar process. In order to avoid tension on the mucoperiosteal flap, a periosteal horizontal incision was made to increase the length of the flap. The mucoperiosteal flap was then closed with single sutures. All patients were mobilised early, no later than the day following the operation and discharged from hospital on the second or third day after surgery. The patients were not allowed to wear removable dentures during the first 4–6 postoperative weeks.
Implant surgery
Six months after bone graft surgery, the implant surgery was performed, following the routines of the Bra˚nemark system7, under local anaesthesia and conscious sedation. The bone graft fixation screws were removed at implant surgery. A surgical guide was used to optimise the position of the implants. Thirty-two patients received 8 implants, seven patients 7 implants, two patients 6 implants, two patients 4 implants, and one patient 9 implants. A total of 334 Bra˚nemark machined surface implants were inserted. The implants were supplied with cover screws and left for healing for 6 months before abutment connection.
Prosthetic treatment
After the grafting procedure the patients did not use their dentures for 4–6 weeks. Thereafter the patients were supplied with a new removable dentures. During the healing period, after the grafting surgery, the patients were recalled for individual check ups and, if needed, the dentures were relined with a soft-tissue relining material. After implant surgery, the dentures were again relined. Abutments were attached after a 6-month healing period in most cases. Multi-unit abutments were used but in some patients angled abutments (178) had to be used. In all patients for whom a metal–ceramic bridge was planned, a temporary bridge in acrylic was first fabricated. The temporary bridge was used for 4–8 weeks. The temporary bridge was fabricated with short cantilevers or without cantilevers and with flat cusps to allow gentle occlusion. The permanent metal–ceramic bridge was formed according to the procedures described in the manual. If the bridges were fabricated in gold–acrylic or titanium–acrylic no temporary bridge was made; this procedure was used for most cases. In patients who lost implants, a decision was made whether to install supplementary implants. Depending on which implant had been lost, the position of the remaining implants, the dentition in the opposing jaw and individual factors such as loading, functional habits and cantilever length played an important roll in determining if supplementary implants should be inserted. If so, a temporary bridge was fabricated reinforced with Kevlar1 threads, and ordinary gold cylinders were used in the acrylic material. The temporary bridge was then used for the additional healing period for approximately 6 months.
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A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla After delivery of the final bridge the patients were instructed in oral hygiene and an individual recall programme was set up. Radiographic and clinical examinations
The patients were examined according to the protocols used at the Departments of Oral & Maxillofacial Surgery and Prosthetic Dentistry, Umea˚ University. Preoperatively, radiographic examination consisted of intraoral images, lateral cephalograms, panoramic radiograms and tomograms. The bone volume was evaluated at every implant site, and patients designated as class IV or V using the CAWOOD and HOWELL8 classification were included in this study. After implant surgery, the patients were followed-up annually and clinically examined. The patients were radiographically examined annually for 5 years and then at 10 years. The intraoral images were taken and adjusted to optimise the parallel technique for each patient’s anatomy. Marginal bone loss was defined as the distance from the junction between the implant and its abutment, to the bone level measured on the mesial and distal surfaces on the implant. A loupe with a magnification factor of 7 and scaled in tenths of millimetres was used. The distance over 5 threads of the implant on the film was measured and divided by the real distance of 3.0 mm and thus revealed the variation in magnification in the intraoral radiographs. The resulting magnification factor for each implant and examination was used to transform the measured radiographic changes of bone level into real bone loss. The mean value of the bone level on the distal and the mesial surface on the implant was used. Statistical methods
Implant survival rate was estimated using the Kaplan–Meier method. In order to compare implant survival for different genders and between smokers and nonsmokers the log rank test was used. Bone loss was described by mean values and associated standard errors. Evaluation of differences in marginal bone loss between males and females and between smokers and non-smokers were based on the Wilcoxon signed rank sum test.
Table 1. Kaplan–Meier estimate of implant survival up to 10 years after implant surgery. Years after operation
Survival probability ( SE) 93.1 1.4 93.1 1.4 93.1 1.4 93.1 1.4 93.1 1.4 90.0 2.0
1 2 3 4 5 10
Table 2. Implant failure after implant surgery, by gender and smoking status. No. of implants
No. of failures
10-year survival
P value*
Males Females
111 223
3 (2.9%) 24 (10.3%)
97.1% 86.4%
0.017
Non smoker Smoker
245 89
16 (6.5%) 11 (12.4%)
93.5% 78.5%
0.072
*
Log rank test.
estimated implant success rate of 90% (Table 1). Twenty-three were early (before loading) failures and 4 were late (after loading) failures. The 4 late failures appeared after 5 years in one patient; a smoker. Gender
The failures were distributed in 17 patients; 2 males and 15 females. Three implants of 111 were lost in males (3%) and 24 of 223 implants in females (10%). This difference in implant failure rate between females and males was statistically significant (p < 0.05, Table 2). Smoking habits
The number of non-smoking patients was 32, including 5 patients defined as ‘previous smokers’; 20 women and 12 men.
Twelve patients were active smokers at the start of this study; 9 women and 3 men. In the non-smoking group there were 16 failures out of 245 (7%) and in the smoking group 11 out of 89 (12%). The proportion of failures was higher among smokers than non-smokers but there was no significant difference between the groups (Table 2). Marginal bone loss
The marginal bone loss, calculated from intraoral radiograms 1 year after implant surgery, was 1.8 mm. Thereafter, the marginal bone levels were 2.1, 2.1, 2.2, 2.3 and 2.4 mm at 2, 3, 4, 5 and 10 years after implant surgery (Table 3, Fig. 1). For all patients, except three, complete follow-up regarding marginal bone loss was available until 5 years after implant surgery. Of the three patients without complete fol-
Table 3. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE). 1 year 1.83 0.05 *
2 year
3 year
4 year
5 year
10 year
2.14 0.05 **
2.08 0.05
2.17 0.05 **
2.25 0.04 **
2.37 0.07
Significantly different from previous time point, p < 0.05. Significantly different from previous time point, p < 0.01.
**
Results Success rate
Of the 334 inserted implants in 44 patients, 27 failed in 17 different patients giving an
Fig. 1. Mean marginal bone loss (in mm) in all patients at different examination times.
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Table 4. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE) by smoking status. Examination 1 year 2 year 3 year 4 year 5 year 10 year *
Non-smoker
Smoker
Mean bone loss SE
Mean bone loss SE
1.75 0.06 2.07 0.06 2.02 0.06 2.10 0.05 2.20 0.04 2.38 0.08
2.02 0.07 2.39 0.11 2.22 0.09 2.40 0.09 2.42 0.07 2.34 0.14
P value* 0.001 0.004 0.049 0.013 0.002 0.800
Wilcoxon rank sum test.
Table 5. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE) by gender. Examination 1 year 2 year 3 year 4 year 5 year 10 year *
Male
Female
Mean bone loss SE
Mean bone loss SE
1.86 0.10 2.15 0.11 2.15 0.11 2.31 0.09 2.38 0.07 2.60 0.12
1.82 0.06 2.13 0.06 2.04 0.05 2.10 0.05 2.18 0.04 2.23 0.07
P value* 0.548 0.826 0.538 0.040 0.036 0.003
Wilcoxon rank sum test.
low-up, one died and two had emigrated before the 5-year examination. Evaluating the marginal bone loss among smokers and non-smokers separately, a significantly greater bone loss was observed among smokers at each examination up to and including the 5year examination (Table 4). At the time of this study, a smaller fraction of the patients (19 of 44) had reached the10-year point so there was only a small number of implants in the smoking group from which to make a prediction. Evaluating the marginal bone loss among females and males separately, a significantly higher bone loss was observed among males at 4, 5 and 10 years (Table 5). Discussion
Patients suffering from maxillary atrophy are in a severely compromised oral situation and in many cases rehabilitation is arduous. The introduction of dental implants, if the bone volume is adequate, allows some of these problems to be solved. In many patients it is necessary to reconstruct the maxilla prior to rehabilitation with implant bridges. Grafting techniques have been developed and improved. The different augmentation techniques are normally based on the classification of the resorption of the alveolar crest by CAWOOD and HOWELL8. In patients who develop a severe alveolar resorption (class VI8) with an endpoint with reversed intermaxillary relationships and/or increased intermax-
illary distance, a Le Fort I osteotomy in combination with an interpositional bone graft and later placements of implants, is preferable. This method also contributes to improved postoperative facial morphology. In patients in whom the resorption results in a high but thin alveolar crest (class IV8) and with acceptable intermaxillary relations, the onlay graft is a better alternative. The first group of patients in this category, treated for maxillary atrophy with bone grafts and implants, have been reported earlier20. Resorption of the bone graft using the onlay technique mainly takes place during the first 12 months21– 23 . In this group of patients, reported earlier, a few patients lost implants owing to extensive bone graft resorption during the initial healing period. To overcome this problem, bone grafts with mainly cortical content were harvested to ensure enough bone volume with sufficient density after the healing of the graft10. This change in treatment protocol in the present study resulted in markedly improved graft healing results. This study was performed in a twostage procedure to allow more predictable positioning of the implants and an increased implant success rate18,21,28,33,34. YERIT et al.34 compared the one- and twostage techniques at a 5-year follow-up and found survival rates of 87% and 91%, respectively. SJO¨STRO¨M et al.28 showed a significantly greater survival rate for delayed implant placement compared with simultaneous implant placement when
using additional test implants retrieved after 6 months from the bone grafts. The overall estimated implant success rate in this prospective study was 90%. This is in accordance with a 15-year follow-up by JeMT and JOHANSSON14 who found similar long-term success rates after implant treatment in the edentulous maxillae in nongrafted patients. A survey of the literature on similar grafting technique as in the present study, reports survival rates varying from 49 to 95%15,22,26,27,29,32. The time in long-term follow-up studies varies from 12 to 124 months26; only one study covered a minimum of 10 years22. Other studies compare the implant survival rate in grafted areas as compared with non-grafted areas4,33. In these studies the survival rate was greater in the nongrafted areas; 84–87% compared with 74– 75% in the grafted areas. Females lost significantly more implants in the present study (Table 2). SCHLIEPHAKE et al.27 and SJO¨STRO¨M et al.29 showed a lower success rate in women, and the present study confirms their results. Smoking did not significantly affect the implant success rate in this study, but the number of failed implants among smokers indicates that there is a relation between smoking and implant failure. This has been reported by many authors2,9,11,15,32,33, and smoking must be considered a risk for implant survival. The overall marginal bone level was reduced during follow-up from 1.8 mm at the 1-year follow-up, to 2.4 mm after 10 years. That represents a mean bone loss of 0.55 mm from the first examination at 1 year after surgery to the 10-year examination (Fig. 1). This is in agreement with the marginal bone loss around maxillary implants reported by JEMT and JOHANSSON14 in non-grafted patients. They showed a mean marginal bone loss of 0.5 mm after 5 years and only minimal changes in marginal bone during the following 10 years. HALLMAN et al.12 compared two different implant systems in grafted patients using interpositional bone grafts and found a marginal bone loss of 2.3–2.4 mm after 5 years. In a 3-year report by SJO¨STRO¨M et al.29 the mean marginal bone loss was 1.9 0.4 mm apical to the reference level at the radiographic examination 1 year after implant placement. The change in marginal bone level, from the first radiographic examination to the 3-year time point29, was 0.3 0.3 mm. The marginal bone loss is most pronounced during the first year and changes little thereafter12,22,29,30. Men lost significantly more marginal bone than women in the long term. During
A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla the first 3 years there was no significant difference but after the 4-year examination there was a continuing increase in bone loss in men compared with women. Females lose significantly more implants but men lose more marginal bone. The explanation might be differences in bone quality. This is an issue to be explored further. In the present study, the marginal bone level also differed significantly between smokers and non-smokers. There was a statistically significant difference between the groups at all of the annual observations except at the 10-year examination where the number of implants among the smokers was very small. LINDQUIST et al.19 studied the association between marginal bone loss and smoking habits around mandibular implants (routine patients) in a 10year follow-up. They showed a greater bone loss in smokers, especially in smokers with poor oral hygiene, compared with non-smokers, in whom the bone loss was very small. Smoking patients lose more implants as well as marginal bone level. The impact of smoking is serious2,11,15 and the impact must be considered when considering treatment involving grafting procedures. The residual bone in the alveolar crest is of importance concerning the survival rate of the implants4,11,15,18. Where there is more residual bone, the survival rate can be expected to be higher than where there is less residual bone in the alveolar crest. As a consequence, patients in classes V and VI can be expected to have a higher risk for implant failure4 than patients designated as class IV. Loading forces from the mandibular dentition have a great impact on maxillary resorption prior to reconstruction and bone graft healing and implant survival3,15,22,26. In this study, the patients were either supported by mandibular dentition/ implant supported bridges or they had anterior teeth with or without removable dentures, occluding to the upper jaw. Only one patient was edentate, wearing a removable denture at the start of the treatment. Loading from the mandibular teeth should be avoided during the healing time3,15,23. In patients where the mandibular anterior teeth have a possibility to occlude to the grafted area, a splint was fabricated. The patients were advised to wear the splint 24 hours/day for the first 2 weeks and thereafter only when asleep until a new denture was fabricated. This reduced the loading factor until stabilisation of the graft had occurred20,25. Most patients in this study had been edentate for 25–40 years; this was reported
by TALLGREN31 who showed an increased resorption in the jaws over time. Increased knowledge of the problems encountered in this type of patient enhances treatment outcome in the maxilla and at the donor site. Long-term experience is necessary to predict treatment outcome and prognosis. The reconstruction of atrophic maxillae with bone grafts from the iliac crest and placement of endosseous implants in the healed graft is a predictable technique to facilitate rehabilitation of the atrophic edentulous maxillae.
12.
13.
14.
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bilitation of patients with severely resorbed maxillae by means of implants with or without bone grafts. A 3- to 5-year follow-up clinical report. Int J Oral Maxilllofac Implants 2001: 16: 73–79. 34. Yerit KC, Posch M, Guserl U, Turhani D, Schopper C, Wanschitz F, Wagner A, Watzinger F, Ewers R. Rehabilitation of the severely atrophied maxilla by horseshoe Le Fort I osteotomy (HLFO). Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004: 97: 683–692. ˚ strand P, Nord PG, Bra˚nemark PI. 35. A Titanium implants and onlay bone graft to the atrophic edentulous maxilla: a 3-year longitudinal study. Int J Oral Maxillofac Surg 1996: 25: 25–29. Address: Elisabeth Nystro¨m Department of Oral & Maxillofacial Surgery Umea˚ University S-90187 Umea˚ Sweden Tel: +46(0)907856113 Fax: +46(0)90773174 E-mail: [email protected]
Leading Clinical Paper Pre-Implant Surgery
A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla
E. Nystro¨m1, H. Nilson2, J. Gunne2, S. Lundgren1 1 Department of Oral Maxillofacial Surgery, Umea˚ University, Umea˚, Sweden; 2 Department of Prosthetic Dentistry, Umea˚ University, Umea˚, Sweden
E. Nystro¨m, H. Nilson, J. Gunne, S. Lundgren: A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla. Int. J. Oral Maxillofac. Surg. 2009; 38: 111–116. # 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Treatment of the atrophic edentulous maxilla is challenging especially when bone graft procedures are necessary. In this study an onlay bone graft, a saddle or veneer, with or without maxillary sinus floor inlay graft, harvested from the anterior iliac crest, in combination with implants was used in the reconstruction of patients with extreme atrophy in their maxillae. The aim was to investigate treatment outcome, and the impact of gender and smoking, in 44 patients in a prospective, long-term, follow-up study concerning implant survival rate and marginal bone loss adjacent to the surfaces of the implant. Mean follow-up time was 11 years. Of 334 inserted Bra˚nemark implants, with machined surface, 27 failed. Estimated implant survival rate was 90%. Marginal bone loss was 1.8 mm 1 year after implant surgery; 2.3 mm after 5 years; and 2.4 mm after 10 years. There was a significant difference between genders in implant survival. Marginal bone loss differed significantly between smokers and non-smokers up to the 5-year examination and between genders after the 4-year examination. The onlay bone graft, with or without a maxillary inlay graft, results in high implant survival rate, good oral function and stabilised marginal bone. All patients are still wearing their original fixed bridges.
In the atrophic edentulous maxilla, grafting procedures in combination with endosteal implants are necessary1,5,6,13,16,17,24,35. The final physiological resorption differs between patients, so different reconstructive techniques should be used, for example, in the thin alveolar process a saddle or veneer onlay graft can be chosen20, while if there are reversed intermaxillary relations or an increased vertical distance between the maxilla and mandible, an interposi0901-5027/020111 + 06 $30.00/0
tional bone graft and Le Fort I osteotomy is an alternative25. One requirement for successful treatment with endosteal implants is a sufficient amount of jaw bone. In patients with advanced resorption of the maxilla this bone is not available, therefore augmenting procedures to reconstruct the alveolar crest to increase the vertical and horizontal dimensions are necessary.
Keywords: bone grafting; autogenous bone; iliac crest; maxilla; implants; marginal bone level. Accepted for publication 28 October 2008 Available online 28 November 2008
The aim of reconstruction with bone grafts and implants is to restore facial morphology. The condition of the alveolar crest determines the choice of surgical technique to optimize function and appearance for the patient. The anterior iliac crest is a common donor site, especially when both cortical and cancellous bone are required. The medial table has a thin cortical plate compared with the superior or lateral borders of the iliac
# 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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crest. The area of the lateral iliac crest, where the medial gluteus muscle inserts, known as the tubercle, contains cortical bone with a high density and thickness. This area is preferable when large amounts of cortical bone are needed. The disadvantage of harvesting bone from the superior or lateral border of the iliac crests is that interference with the insertion of the gluteus muscles may cause gait disturbance10. The aims of this study were to evaluate the implant survival rate and marginal bone level after long-term follow-up and to study the impact of smoking and gender on these aspects.
Material and methods
This study comprised 44 consecutive edentate patients with maxillary atrophy, 15 men and 29 women. The patients were referred to the Department of Oral and Maxillofacial Surgery, Umea˚ University Hospital, for reconstruction of the maxillary alveolar ridge with bone grafts and implants. The mean age of the patients was 58 years (range 45–68 years). This group of patients was followed annually with a mean follow-up time of 11 years (range 9– 14 years) after the implant surgery. The patients in this study suffered from severe maxillary atrophy verified by clinical and tomographic examination. Most patients had sufficient bone height, but not sufficient width in the maxilla for implant treatment; class IV according to CAWOOD and HOWELL8. Some patients also had inadequate vertical height, more often seen in the anterior maxilla; class V according to CAWOOD and HOWELL8. Of the 44 patients, 24 underwent reconstruction in the anterior and posterior maxilla with an onlay bone graft; a veneer graft in the posterior maxilla and a veneer or saddle graft in the anterior maxilla. The remaining 20 patients had reconstruction with an onlay bone graft in the anterior maxilla and an inlay bone graft in the maxillary sinus floor bilaterally. Vertical augmentation of the nasal floor was performed with an onlay bone graft in 40 of the 44 patients. The 29 female patients received 223 implants and the 15 men received 111 implants. Twenty-seven patients were non-smokers and 5 patients had previously smoked but had stopped smoking before surgery; 12 patients were active smokers. In the smoking group of 12 patients 89 implants were inserted and in the nonsmoking group of 32 patients received 245 implants.
The patients had been edentate for a long time: 32 patients for more than 25 years (25–48 years), 4 patients for 10–25 years, and 7 patients for up to 10 years. Edentate duration was not reported for one patient. Of 44 patients, 22 were dentate or supported with an implant-supported fixed bridge in the mandible and 21 patients had an anterior dentition with or without removable prostheses. Only one patient in the study was edentate.
Reconstructive surgery
Surgery was performed under general anaesthesia with oral endotracheal intubation. A local anaesthetic with a vasoconstrictor was used for haemostasis. Bensylpenicillin, 3 g, were administered at the start of the operation. The iliac crest was chosen as the donor site. A corticocancellous block was harvested from the superolateral border of the iliac crest. The bone grafts were stored in blood-soaked gauze. The wound was closed in layers; the closure of the first layer, the fascia lata, was carefully readapted to avoid marrow bone bleeding into surrounding soft tissue. An activated vacuum drainage was positioned between the fascia lata and the muscles and kept in place until bleeding stopped, usually on the second postoperative day. The skin was closed with continuous intracutaneous sutures using resorbable material. Intraorally, a mucoperiosteal flap, labially directed through a midcrestal incision, was raised to expose the lateral wall of the sinus, nasal aperture and the anterior maxillary alveolar crest. The surgical bone-grafting procedure, preparation of the sinuses, and elevation of the sinus and nasal mucosa have been described previously20. The bone grafts were placed in the sinuses as well as on the anterior nasal floor and as veneer or saddle grafts on the alveolar ridge. The cortiococancellous bone blocks were adjusted and placed on the alveolar process and rigidly fixed with titanium screws (2 mm diameter). Each bone block was rigidly fixed with 2–3 screws engaging the total residual alveolar process. In order to avoid tension on the mucoperiosteal flap, a periosteal horizontal incision was made to increase the length of the flap. The mucoperiosteal flap was then closed with single sutures. All patients were mobilised early, no later than the day following the operation and discharged from hospital on the second or third day after surgery. The patients were not allowed to wear removable dentures during the first 4–6 postoperative weeks.
Implant surgery
Six months after bone graft surgery, the implant surgery was performed, following the routines of the Bra˚nemark system7, under local anaesthesia and conscious sedation. The bone graft fixation screws were removed at implant surgery. A surgical guide was used to optimise the position of the implants. Thirty-two patients received 8 implants, seven patients 7 implants, two patients 6 implants, two patients 4 implants, and one patient 9 implants. A total of 334 Bra˚nemark machined surface implants were inserted. The implants were supplied with cover screws and left for healing for 6 months before abutment connection.
Prosthetic treatment
After the grafting procedure the patients did not use their dentures for 4–6 weeks. Thereafter the patients were supplied with a new removable dentures. During the healing period, after the grafting surgery, the patients were recalled for individual check ups and, if needed, the dentures were relined with a soft-tissue relining material. After implant surgery, the dentures were again relined. Abutments were attached after a 6-month healing period in most cases. Multi-unit abutments were used but in some patients angled abutments (178) had to be used. In all patients for whom a metal–ceramic bridge was planned, a temporary bridge in acrylic was first fabricated. The temporary bridge was used for 4–8 weeks. The temporary bridge was fabricated with short cantilevers or without cantilevers and with flat cusps to allow gentle occlusion. The permanent metal–ceramic bridge was formed according to the procedures described in the manual. If the bridges were fabricated in gold–acrylic or titanium–acrylic no temporary bridge was made; this procedure was used for most cases. In patients who lost implants, a decision was made whether to install supplementary implants. Depending on which implant had been lost, the position of the remaining implants, the dentition in the opposing jaw and individual factors such as loading, functional habits and cantilever length played an important roll in determining if supplementary implants should be inserted. If so, a temporary bridge was fabricated reinforced with Kevlar1 threads, and ordinary gold cylinders were used in the acrylic material. The temporary bridge was then used for the additional healing period for approximately 6 months.
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A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla After delivery of the final bridge the patients were instructed in oral hygiene and an individual recall programme was set up. Radiographic and clinical examinations
The patients were examined according to the protocols used at the Departments of Oral & Maxillofacial Surgery and Prosthetic Dentistry, Umea˚ University. Preoperatively, radiographic examination consisted of intraoral images, lateral cephalograms, panoramic radiograms and tomograms. The bone volume was evaluated at every implant site, and patients designated as class IV or V using the CAWOOD and HOWELL8 classification were included in this study. After implant surgery, the patients were followed-up annually and clinically examined. The patients were radiographically examined annually for 5 years and then at 10 years. The intraoral images were taken and adjusted to optimise the parallel technique for each patient’s anatomy. Marginal bone loss was defined as the distance from the junction between the implant and its abutment, to the bone level measured on the mesial and distal surfaces on the implant. A loupe with a magnification factor of 7 and scaled in tenths of millimetres was used. The distance over 5 threads of the implant on the film was measured and divided by the real distance of 3.0 mm and thus revealed the variation in magnification in the intraoral radiographs. The resulting magnification factor for each implant and examination was used to transform the measured radiographic changes of bone level into real bone loss. The mean value of the bone level on the distal and the mesial surface on the implant was used. Statistical methods
Implant survival rate was estimated using the Kaplan–Meier method. In order to compare implant survival for different genders and between smokers and nonsmokers the log rank test was used. Bone loss was described by mean values and associated standard errors. Evaluation of differences in marginal bone loss between males and females and between smokers and non-smokers were based on the Wilcoxon signed rank sum test.
Table 1. Kaplan–Meier estimate of implant survival up to 10 years after implant surgery. Years after operation
Survival probability ( SE) 93.1 1.4 93.1 1.4 93.1 1.4 93.1 1.4 93.1 1.4 90.0 2.0
1 2 3 4 5 10
Table 2. Implant failure after implant surgery, by gender and smoking status. No. of implants
No. of failures
10-year survival
P value*
Males Females
111 223
3 (2.9%) 24 (10.3%)
97.1% 86.4%
0.017
Non smoker Smoker
245 89
16 (6.5%) 11 (12.4%)
93.5% 78.5%
0.072
*
Log rank test.
estimated implant success rate of 90% (Table 1). Twenty-three were early (before loading) failures and 4 were late (after loading) failures. The 4 late failures appeared after 5 years in one patient; a smoker. Gender
The failures were distributed in 17 patients; 2 males and 15 females. Three implants of 111 were lost in males (3%) and 24 of 223 implants in females (10%). This difference in implant failure rate between females and males was statistically significant (p < 0.05, Table 2). Smoking habits
The number of non-smoking patients was 32, including 5 patients defined as ‘previous smokers’; 20 women and 12 men.
Twelve patients were active smokers at the start of this study; 9 women and 3 men. In the non-smoking group there were 16 failures out of 245 (7%) and in the smoking group 11 out of 89 (12%). The proportion of failures was higher among smokers than non-smokers but there was no significant difference between the groups (Table 2). Marginal bone loss
The marginal bone loss, calculated from intraoral radiograms 1 year after implant surgery, was 1.8 mm. Thereafter, the marginal bone levels were 2.1, 2.1, 2.2, 2.3 and 2.4 mm at 2, 3, 4, 5 and 10 years after implant surgery (Table 3, Fig. 1). For all patients, except three, complete follow-up regarding marginal bone loss was available until 5 years after implant surgery. Of the three patients without complete fol-
Table 3. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE). 1 year 1.83 0.05 *
2 year
3 year
4 year
5 year
10 year
2.14 0.05 **
2.08 0.05
2.17 0.05 **
2.25 0.04 **
2.37 0.07
Significantly different from previous time point, p < 0.05. Significantly different from previous time point, p < 0.01.
**
Results Success rate
Of the 334 inserted implants in 44 patients, 27 failed in 17 different patients giving an
Fig. 1. Mean marginal bone loss (in mm) in all patients at different examination times.
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Table 4. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE) by smoking status. Examination 1 year 2 year 3 year 4 year 5 year 10 year *
Non-smoker
Smoker
Mean bone loss SE
Mean bone loss SE
1.75 0.06 2.07 0.06 2.02 0.06 2.10 0.05 2.20 0.04 2.38 0.08
2.02 0.07 2.39 0.11 2.22 0.09 2.40 0.09 2.42 0.07 2.34 0.14
P value* 0.001 0.004 0.049 0.013 0.002 0.800
Wilcoxon rank sum test.
Table 5. Bone loss defined as distance (in mm) from junction between implant and its abutment to bone level at implant surface (mean SE) by gender. Examination 1 year 2 year 3 year 4 year 5 year 10 year *
Male
Female
Mean bone loss SE
Mean bone loss SE
1.86 0.10 2.15 0.11 2.15 0.11 2.31 0.09 2.38 0.07 2.60 0.12
1.82 0.06 2.13 0.06 2.04 0.05 2.10 0.05 2.18 0.04 2.23 0.07
P value* 0.548 0.826 0.538 0.040 0.036 0.003
Wilcoxon rank sum test.
low-up, one died and two had emigrated before the 5-year examination. Evaluating the marginal bone loss among smokers and non-smokers separately, a significantly greater bone loss was observed among smokers at each examination up to and including the 5year examination (Table 4). At the time of this study, a smaller fraction of the patients (19 of 44) had reached the10-year point so there was only a small number of implants in the smoking group from which to make a prediction. Evaluating the marginal bone loss among females and males separately, a significantly higher bone loss was observed among males at 4, 5 and 10 years (Table 5). Discussion
Patients suffering from maxillary atrophy are in a severely compromised oral situation and in many cases rehabilitation is arduous. The introduction of dental implants, if the bone volume is adequate, allows some of these problems to be solved. In many patients it is necessary to reconstruct the maxilla prior to rehabilitation with implant bridges. Grafting techniques have been developed and improved. The different augmentation techniques are normally based on the classification of the resorption of the alveolar crest by CAWOOD and HOWELL8. In patients who develop a severe alveolar resorption (class VI8) with an endpoint with reversed intermaxillary relationships and/or increased intermax-
illary distance, a Le Fort I osteotomy in combination with an interpositional bone graft and later placements of implants, is preferable. This method also contributes to improved postoperative facial morphology. In patients in whom the resorption results in a high but thin alveolar crest (class IV8) and with acceptable intermaxillary relations, the onlay graft is a better alternative. The first group of patients in this category, treated for maxillary atrophy with bone grafts and implants, have been reported earlier20. Resorption of the bone graft using the onlay technique mainly takes place during the first 12 months21– 23 . In this group of patients, reported earlier, a few patients lost implants owing to extensive bone graft resorption during the initial healing period. To overcome this problem, bone grafts with mainly cortical content were harvested to ensure enough bone volume with sufficient density after the healing of the graft10. This change in treatment protocol in the present study resulted in markedly improved graft healing results. This study was performed in a twostage procedure to allow more predictable positioning of the implants and an increased implant success rate18,21,28,33,34. YERIT et al.34 compared the one- and twostage techniques at a 5-year follow-up and found survival rates of 87% and 91%, respectively. SJO¨STRO¨M et al.28 showed a significantly greater survival rate for delayed implant placement compared with simultaneous implant placement when
using additional test implants retrieved after 6 months from the bone grafts. The overall estimated implant success rate in this prospective study was 90%. This is in accordance with a 15-year follow-up by JeMT and JOHANSSON14 who found similar long-term success rates after implant treatment in the edentulous maxillae in nongrafted patients. A survey of the literature on similar grafting technique as in the present study, reports survival rates varying from 49 to 95%15,22,26,27,29,32. The time in long-term follow-up studies varies from 12 to 124 months26; only one study covered a minimum of 10 years22. Other studies compare the implant survival rate in grafted areas as compared with non-grafted areas4,33. In these studies the survival rate was greater in the nongrafted areas; 84–87% compared with 74– 75% in the grafted areas. Females lost significantly more implants in the present study (Table 2). SCHLIEPHAKE et al.27 and SJO¨STRO¨M et al.29 showed a lower success rate in women, and the present study confirms their results. Smoking did not significantly affect the implant success rate in this study, but the number of failed implants among smokers indicates that there is a relation between smoking and implant failure. This has been reported by many authors2,9,11,15,32,33, and smoking must be considered a risk for implant survival. The overall marginal bone level was reduced during follow-up from 1.8 mm at the 1-year follow-up, to 2.4 mm after 10 years. That represents a mean bone loss of 0.55 mm from the first examination at 1 year after surgery to the 10-year examination (Fig. 1). This is in agreement with the marginal bone loss around maxillary implants reported by JEMT and JOHANSSON14 in non-grafted patients. They showed a mean marginal bone loss of 0.5 mm after 5 years and only minimal changes in marginal bone during the following 10 years. HALLMAN et al.12 compared two different implant systems in grafted patients using interpositional bone grafts and found a marginal bone loss of 2.3–2.4 mm after 5 years. In a 3-year report by SJO¨STRO¨M et al.29 the mean marginal bone loss was 1.9 0.4 mm apical to the reference level at the radiographic examination 1 year after implant placement. The change in marginal bone level, from the first radiographic examination to the 3-year time point29, was 0.3 0.3 mm. The marginal bone loss is most pronounced during the first year and changes little thereafter12,22,29,30. Men lost significantly more marginal bone than women in the long term. During
A 9–14 year follow-up of onlay bone grafting in the atrophic maxilla the first 3 years there was no significant difference but after the 4-year examination there was a continuing increase in bone loss in men compared with women. Females lose significantly more implants but men lose more marginal bone. The explanation might be differences in bone quality. This is an issue to be explored further. In the present study, the marginal bone level also differed significantly between smokers and non-smokers. There was a statistically significant difference between the groups at all of the annual observations except at the 10-year examination where the number of implants among the smokers was very small. LINDQUIST et al.19 studied the association between marginal bone loss and smoking habits around mandibular implants (routine patients) in a 10year follow-up. They showed a greater bone loss in smokers, especially in smokers with poor oral hygiene, compared with non-smokers, in whom the bone loss was very small. Smoking patients lose more implants as well as marginal bone level. The impact of smoking is serious2,11,15 and the impact must be considered when considering treatment involving grafting procedures. The residual bone in the alveolar crest is of importance concerning the survival rate of the implants4,11,15,18. Where there is more residual bone, the survival rate can be expected to be higher than where there is less residual bone in the alveolar crest. As a consequence, patients in classes V and VI can be expected to have a higher risk for implant failure4 than patients designated as class IV. Loading forces from the mandibular dentition have a great impact on maxillary resorption prior to reconstruction and bone graft healing and implant survival3,15,22,26. In this study, the patients were either supported by mandibular dentition/ implant supported bridges or they had anterior teeth with or without removable dentures, occluding to the upper jaw. Only one patient was edentate, wearing a removable denture at the start of the treatment. Loading from the mandibular teeth should be avoided during the healing time3,15,23. In patients where the mandibular anterior teeth have a possibility to occlude to the grafted area, a splint was fabricated. The patients were advised to wear the splint 24 hours/day for the first 2 weeks and thereafter only when asleep until a new denture was fabricated. This reduced the loading factor until stabilisation of the graft had occurred20,25. Most patients in this study had been edentate for 25–40 years; this was reported
by TALLGREN31 who showed an increased resorption in the jaws over time. Increased knowledge of the problems encountered in this type of patient enhances treatment outcome in the maxilla and at the donor site. Long-term experience is necessary to predict treatment outcome and prognosis. The reconstruction of atrophic maxillae with bone grafts from the iliac crest and placement of endosseous implants in the healed graft is a predictable technique to facilitate rehabilitation of the atrophic edentulous maxillae.
12.
13.
14.
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