Long-term effects of vertical bone augmentation: a systematic review

ABSTRACT Extraction, periodontitis, or trauma can cause a reduction on the alveolar ridge. This could result in an insufficient alveolar bone width and height. Different techniques of vertical bone augmentation are described in literature. However, nowadays there is not enough evidence against lateral augmentation procedures to verify if these techniques are stable over a long period of time. Objective This review analyses the different techniques that are used to vertically augment the bone and evaluate if these techniques are stable over a long period of time. Material and Methods The MEDLINE-PubMed database was searched from its earliest records until December 22, 2014. The following search term was used: Alveolar Ridge augmentation [MESH]. Several journals were hand searched and some authors were contacted for additional information. The primary outcome measure that was analyzed was marginal bone level change around dental implants in the augmented sites, and the secondary outcomes were survival and success rates of dental implants placed in the augmented sites. Results The search yielded 203 abstracts. Ultimately, 90 articles were selected, describing 51 studies meeting the eligibility criteria. The marginal bone level change for the inlay technique and vertical guided bone regeneration are in agreement with the success criteria. Alveolar distraction showed more marginal bone level change after the first year of loading, and for the inlay technique very few studies were available. Conclusions Based on the available data in the current existing studies with a follow-up period of at least 4 to 5 years, one can summarize that there seems to be a trend that the onlay technique, alveolar distraction, and vertical guided bone regeneration are stable for at least 4 to 5 years.


INTRODUCTION
Since Brånemark introduced a new dental treatment, a machined titanium implant, a new treatment option became available 3 . If there is sufficient bone quantity and quality, a dental implant could be a predictable treatment option. In literature, a survival rate over 95% in noncompromised patients is reported 32 . Therefore, dental implants have become a reliable treatment option for patients missing one or multiple teeth. However, unfavourable conditions of the alveolar bone due to periodontitis, extraction, or trauma provoke decrease in the alveolar ridge due to bone atrophy. Such bone atrophy could cause challenging interarch relationship in vertical, transverse, and sagittal planes, which may cause incorrect dental implant placement from a functional and aesthetic point of view 19 .
To provide adequate bone volume and to assure an adequate aesthetic result, bone augmentation procedures are sometimes a prerequisite for successful dental implant treatment. There are different techniques to augment the bone, such as: 1. Onlay grafting. The graft material will be placed on top of the defect to increase height or width of the alveolar bone. The graft is immobilised with dental implants, screws, or plates 52 .
2. Inlay grafting. A part of the alveolar ridge is surgically separated and a graft material is placed between the two sections 52 .
3. Ridge expansion. A part of the alveolar ridge is longitudinally split to widen the ridge and allow placement of a graft, an oral implant, or both 35 . 4. Distraction osteogenesis. A gradual, controlled displacement of a surgically prepared fracture. The two bone fragments are slowly pulled apart, and new bone will arise in the gap 26 .
5. Guided bone regeneration (GBR). A space is maintained by a barrier membrane, which will be 67 . Different materials can be used for augmentation: 1. Autogenous bone graft. This bone graft is taken from the same patient in an adjacent or remote site. This material is considered to be the "gold standard", while it is biologically compatible and provides a scaffold for new bone formation 77 .
2. Allograft. This bone graft is harvested from human cadavers and processed by methods such as freezing or demineralising and freezing 67 .
3. Xenograft. This is a graft material derived from animals, usually bovine bone. It is processed to completely remove the organic component 13 . 4. Alloplastic graft. This bone graft is a synthetic bone substitute made up of bioactive glass or calcium phosphates 112 . 5. Osteoinductive material. This material stimulates the osteoprogenitor cells to differentiate into osteoblasts and accelerate new bone formation. The most common are bone morphogenetic proteins (BMPs), platelet rich plasma (PRP), and leukocyte 33 .
Each type of augmentation material may be used combined with a variety of different surgical techniques.
The rationale for the use of a vertical bone augmentation is to improve the vertical dimension of the bone. If the use of a vertical bone augmentation technique is needed, the clinician needs to decide which technique and which material should be used to vertically augment the bone. When the vertical bone augmentation is successful, one can proceed for dental implant placement. The aim of this review is to analyze the success, survival rates of dental implants, and the marginal bone level change around dental implants placed in the augmented area. Marginal bone level change is most often controlled through x-rays in the maintenance phase to demonstrate and secure implant success.

MATERIAL AND METHODS
The following analysis was performed in a different way according to the guidelines of the Cochrane Collaboration and the principles of the PRISMA (Preferred Reporting Items for Systemic Reviews and Meta-Analyses) statement for a systematic review 46,69 .

Study inclusion and exclusion criteria
The selection process was performed by two masked reviewers (OB and JK). The studies were analyzed according to the following inclusion criteria: 1. All studies in which at least 10 patients were treated and had a follow-up of at least 12 months.
2. Patients presenting deficient edentulous ridges caused by atrophy, periodontal disease, and trauma were considered.
3. The following surgical procedures were considered: onlay bone grafts, split-ridge/ridge expansion techniques/inlay technique (vertical direction), alveolar distraction osteogenesis, and guided bone regeneration procedures. 4. Articles related to dental implants were considered for inclusion. 5. No specific dental implant system was excluded.
6. No specific augmentation material was excluded.
7. Only studies in the English language were included.
The following exclusion criteria were used: 1. Patients with bone defects caused by congenital malformations, after ablation of tumors, or osteoradionecrosis.
2. The following surgical procedures were excluded: sinus floor elevation by a lateral approach, Le Fort I osteotomy with interpositional techniques, and correction of dehiscences and fenestrations.

Outcome variables
The primary outcome was: marginal bone level change around dental implants in the augmented sites. The following recall moments were noted: baseline (placement of the final crown, start loading), year 1, 2, 3, 4, and 5 of loading. The secondary outcomes were survival and success rates of dental implants placed in the augmented sites. Implant survival was evaluated using Simonis, et al. 97 (2010), being implant removal the survival criterion. Implant success was evaluated using Albrektsson, et al. 5 (2012), and the success criteria were absence of persistent pain or dysesthesia, absence of peri-implant infection with suppuration, absence of mobility, absence of continuous periimplant radiolucency, less than 1.5 mm of perifunction, and less than 0.2 mm in subsequent years.

Data extraction
The title and abstract of studies with potential relevance for the review were obtained and screened independently by two masked reviewers (OB and JK). Studies without abstract, but with a title suggesting relevance to the subject of the review, were selected for full text screening. The selected full-text articles were independently read in detail to verify whether they passed the inclusion/ exclusion criteria. The references of the full text articles were screened for any relevant additional were processed for data extraction. Discrepancies regarding the inclusion or exclusion of studies were resolved by discussion between the reviewers (OB and JK). The extracted data included: year of publication, design of the study, number of patients per study arm, defect type, surgical procedure, donor site, number of dental implants, timing of implants, follow-up time, primary outcome measure loading), year 1, 2, 3, 4, and 5 of loading, and secondary outcomes measures. The quality of the analysis, therefore, no quality assessment has been done.

Statistical analyses
Data of the included studies were extracted and inserted into a database. Mean values and standard deviations were extracted from the data. If no standard deviation was available, it was recalculated n is the sample size. When mean follow-up period was used, it was recalculated, if possible, for every year; if not, the data available, the corresponding authors were contacted for additional data. The available data were recalculated in order to present the data like marginal bone level change at baseline (placement and 5 of loading, and the latest available data for survival and success rates were noted. The data of this review was statistically analyzed using the program SPSS 21.0 (IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.).

RESULTS
The initial search resulted in a total of 3248 articles ( Figure 1). After screening the titles, 203 abstracts were included for further analysis. Analysis of the abstracts resulted in 90 potential articles. In the third phase, the full-text articles of the remaining 90 articles were evaluated, of which 39 articles 2,8,9,12,14,18,23,24,27,28,30,39,41,44,45,48,49,51,56,59,60,62,64,68,73,75,84,89,90,[92][93][94]98,102,103,107,108,111,113 did not pass the inclusion criteria ( Figure 2). A screening of the reference lists of the full text articles did not result in any additional articles. In Table 1 . Only the treatment groups of interest are represented. For vertical bone augmentation, four different techniques were used and the results will be presented separately. In Table 2, the characteristics of the different vertical augmentation techniques are presented.

Alveolar distraction (Table 1, Figure 3)
T h e 5 1 i n c l u d e d a r t i c l e s p r ov i d e d 1 7 studies 10,21,22,25,36,37,40,43,50,57,79,[81][82][83]95,104,114 with alveolar distraction, and one study 86 used a combination of the inlay technique and alveolar distraction. Eight studies were retrospective while 10 were prospective. A total of 333 patients with a vertical resorption of partially or totally edentulous alveolar ridges were treated with intraoral intraosseous or extraosseous devices. Twelve patients were treated with a combination of inlay technique and vertical distraction. In total, 1011 dental implants were placed after 3 to 6 months, and the mean was 3.8 months after the completion of the distraction. After the start of loading, the follow-up ranged from 1 to 7.1 years and the mean was 2.9 years. The survival rates for the dental implants in alveolar distracted bone ranged from 88 to 100% and the mean was

Reason for exclusion
Useful clinical results, more information needed. Could

Sinus elevation was included in study group
Sinus elevation was included in study group

Inlay technique (Table 1, Figure 4)
The 51 articles included provided four studies 10,38,42,53 with inlay technique, and one study 85 used a combination of onlay and inlay techniques. Of these, two were prospective studies; one, a a split mouth study; and one, a randomized clinical trial. A total of 57 patients with a vertical resorption of partially or totally edentulous alveolar ridges were treated with the inlay technique. Seventeen patients were treated with a combination of onlay and inlay techniques. Three different donor materials for the bone where used: autogenous (iliac 10,42 , ramus 53 ), xenografts 38 , and alloplastic grafts 53 . In total, 206 dental implants were placed after 3 to 6 months, and the mean was 4.6 months after the healing of the inlay technique. After the start of loading, the follow-up ranged from 1 to 3 years, and the mean was 1.7 years. Survival rates for the dental implants in bone from the inlay technique ranged from 95.9 to 100.0%, and the mean was 98.5%. Unfortunately, only four studies evaluated the implant success rate, which ranged from 90.9 to 100.0%, and the mean was 93.4%.
Only eight studies 15,20,25,29,31,42,57,74   Vertical guided bone regeneration (Table 1, Figure 6) The 51 articles included provided seven s t u d i e s 6 , 2 2 , 6 1 , 8 0 , 9 6 , 1 0 0 , 1 0 5 w i t h v e r t i c a l b o n e regeneration. Three studies were retrospective while 4 were prospective. A total of 138 patients with a vertical resorption of partially or totally edentulous alveolar ridges were treated with vertical guided bone regeneration. Two different donor materials for the bone were used: autogenous (ramus 22,96,105 and chin 96,105 ) and allografts 61,100 . Moreover, combinations of different donor materials for the bone were used -autogenous+allograft 6 and autogenous+xenograft 80 . In total, 141 dental implants were placed immediately, 206 dental implants were placed after 4 to 12 months, and the mean was 7.8 months after the healing of the vertical bone regeneration. After the start of loading, the follow-up ranged from 1.0 to 5.3 years, and the mean was 2.4 years. The survival rates for the dental implants in bone from the vertical bone regeneration ranged from 94.1 to 100.0%, and the mean was 99.3%. The implant success rate ranged from 75.0 to 100.0%, and the mean was 90.7%.
All the seven studies 6

DISCUSSION
In the literature, evidence is available about the stability of vertical bone augmentation. A wide range of different techniques was used to vertically augment the bone. This review tried to systematically evaluate the current evidence and to compare the different vertical augmentation techniques as well as their marginal bone level change on the long-term. In total, 51 articles could be included, from which the data were obtained. Only 21 articles out of 51 contained information about the marginal bone level change. Line graphs with standard deviation were used to present the marginal bone level change over a long period of time.
Few articles 4,5,17,101 showing the marginal bone level change around a successful implant are available in literature. In order to assess the stability of an implant in augmented bone, it is important to know the marginal bone level change around a successful implant in non-augmented bone. The most recent data about marginal bone level change around non-augmented implants were discussed at the Third EAO consensus conference. In this article, data of implants in an augmented side were collected and compared with the EAO consensus conference conclusions.

Alveolar distraction
The analysis shows that the implant survival and success rates are comparable with dental implants which are placed in non-augmented bone 4 5,17 . In the 2 nd , 3 rd , 4 th , and 5 th year, the bone loss is, in most of the studies, more than 0.1 mm. This could indicate that the resorption rate is more rapidly progressing compared to nonaugmented bone.
Alveolar distraction initiates natural bone formation between the distracted segment and the basal bone. Therefore, there is no need for bone grafting, but for a narrow ridge instead. For a narrow ridge, a bone grafting is better to use, since it can rebuild the horizontal and vertical components. Alveolar distraction seems to be only indicated for the mandible because of the pneumatisation of the sinus in the maxilla. A disadvantage of this technique is the early resorption of the distracted bone. It is essential to consider some overcorrection during treatment planning for directly avoiding surgical relapse and another surgical intervention for additional augmentation. Alveolar distraction undergoes a more active remodeling process because of the better vascularization when compared to a block graft 47 . For the long-term, the marginal bone level change might be more stable.

Inlay technique
The analysis shows that implant survival and success rates are comparable with dental implants which are placed in non-augmented bone 4 . The supply to the bone segment which is cranially displaced. The risk of wound dehiscence could arise when there is too much tension after wound closure. Unfortunately, no long-term follow-up studies are available. Therefore, a comparison with dental implants in non-augmented bone is not possible.

Onlay technique
The analysis shows that implant survival and success rates are comparable with dental implants which are placed in non-augmented bone. The line graph ( Figure 4) shows an overview of the marginal studies present the results for a follow-up period of 4 or 5 years 25,29,57,74 . Unfortunately, it was not possible to combine those results. The marginal bone level change between abutment connection and 1 st year of loading varies between -0.60 --1.46 mm; after the 2 nd year, between -0.03 -0.30 mm; after the 3 rd year, between -0.03 --1.03 mm; after the 4 th year, between 0.2 --0.06 mm; and after the 5 th year of loading, between 0.08 --0.27 mm. These data are in agreement with the present success criteria for the 1 st year of loading, which allows a marginal bone loss of 1-1.5 mm, and of 0.1 mm for the 2 nd , 3 rd , 4 th , and 5 th year 5,17 . However, one study 74 showed more marginal bone loss in comparison with others 25,29,57 .
The onlay technique is done mostly with an autogenous bone graft. Before the year 2000, most implants were immediately placed together with the bone grafts. The implants were used to secure the graft. The capacity and volume of the bone grafts are variable between the studies. These differences could be explained by different follow-up periods, timing of implants placement, different sites, and different bone grafting material.
year, but stabilizes after it. The autogenous bone graft is still the most frequently used graft for the onlay technique. It is a recommendation to use corticocancellous bone instead of particulated bone grafts. Ideally, oversized grafts should be harvested to maintain enough volume after the the onlay technique is the management of the soft tissues to maintain a full wound closure. For the long-term, it seems that the marginal bone level change is comparable with dental implants in nonaugmented bone.

Vertical guided bone regeneration
The analysis shows that the implant survival is comparable whereas the success rate is not comparable with dental implants which are placed in non-augmented bone. The line graph ( Figure  5) shows an overview of the marginal bone level present the results for a follow-up period of 5 years 96,105 . Unfortunately, once again it is not possible to combine those results. The marginal bone level change between abutment connection and 1 st year of loading varies between -1.01 --1.86 mm; after the 2 nd year, between 0.05 --0.02 mm; after the 3 rd year, between 0.11 --0.06 mm; after the 4 th year, between 0.27 --0.02 mm; and after the 5 th year of loading, between 0 --0.22 mm. These data are in agreement with the present success criteria for the 1 st year of loading, which 1-1.5 mm, and of 0.1 mm for the 2 nd , 3 rd , 4 th , and 5 th year 5,17 . However, one study 96 has a different amount of dental implants during the follow-up Vertical guided bone regeneration implies that the regeneration of osseous defects is predictably attainable via the application of occlusive membranes, which mechanically exclude non-osteogenic cell populations from the surrounding soft tissues. In the past, nonresorbable membranes were used, but nowadays resorbable membranes are common. The defect and sometimes mixed with xenograft or allograft. Wound dehiscence is often seen as a complication. Therefore, it is important to get as little traction on the wound as possible. For the long-term, it seems that the marginal bone level loss is comparable with dental implants in non augmented bone.
In the literature, a lot of different criteria is used to determine the survival and success rates of dental implants. The lack of universally accepted success criteria makes the interpretation 76 . In addition, a statistical problem is perceived. There is a discrepancy in reported outcomes when the primary unit of analysis is the patient instead of the dental implant 87, 88 . Therefore, the decision is made to show all the data which criterion or statistical analysis has been used. This could be a disadvantage, but it gives the clinician a complete overview of the available literature.
Some new guidelines were proposed in the VIII European Workshop on Periodontology. A successful dental implant has to meet criteria concerning tissue physiology (osseointegration), function (chewing), absence of pain, and user satisfaction 101 criteria for marginal bone loss exist since 1986 5 . This review shows that the marginal bone loss after varies between 1.0 and 1.5 mm. This is called saucerisation, and is caused by the establishment of the biological width. Recent studies allow a mean loading, and an annual of 0.1 mm bone loss can be expected in the following years 17 . The criteria are divided into three domains that are important for identifying the success of a dental implant. These domains are: patient-reported outcome measures (health-related quality of live and general satisfaction), peri-implant health (marginal bone level, bleeding on probing, and probing depth), and implant-supported restorations (longevity of the restoration, function/occlusion related outcomes, and technical complications) 101 .
To give a complete overview about the different techniques, every type of grafting material was included. Depending on the grafting material used, a different resorption occurs. That is why the results are presented in graphs and tables, which facilitates the decision of clinicians regarding what type of grafting material must be used. No distinction is made between the different durations of the follow-up period, even though there was a wide range of it. The follow-up period needs to be of at least one year. These different lengths of follow-up periods are included in the calculations. However, an implant success rate of 100% after one year cannot be compared with a success rate after 10 years. Furthermore, different follow-up periods per patient in a study are pooled together. This could lead to a complete different outcome. This review is designed to give a complete overview, thus, the clinician can decide what the best treatment is.
After analysis of the articles about vertical bone augmentation, the main conclusion was that a wide range of different techniques and materials were used, and also different patient groups, study designs, antibiotic prescriptions, and follow-up regimes. Because of this, no meta-analysis was conducted, for once a meta-analysis is performed, it causes a bias.
Another limitation of this review is that it was not possible to separate the data for single tooth gap, multiple missing teeth, or an edentulous ridge in the different articles used. These different clinical situations were mostly pooled together; therefore, especially in the atrophic jaws, the description of the seize of the defect was hardly present, which was also a topic in the last ITI Consensus Conference 11 . state which vertical bone augmentation is the best to use. However, when only considering those vertical bone augmentation techniques for which studies exist with a follow-up period of at least 4 to 5 years, there seems to be a trend that the onlay technique, alveolar distraction, and vertical guided bone regeneration are stable for at least 4 to 5 years. Since it was not possible to carry out metaanalytic procedures, a conclusion about stability is More studies that follow the marginal bone level change for a longer period are necessary, in addition to better description and ridge measurements of the clinical situation before and after the augmentation procedure. This will enable a better interpretation of the results and allow the clinician to conclude in which clinical situation.