Review article 1

A literature-based comparison of bone augmentation materials and techniques, including alternative methods for restoring the atrophic jaw with implants
Farah Aga
An atrophic jaw is the most common indication for preimplant surgery. Preimplant surgery facilitates the placement of implants of appropriate size in ideal positions in the jaw. It also may be carried out prior to implant placement in instances of surgical resection of the jaw, trauma, developmental malformation and avoidance of important structures such as the maxillary antrum or inferior alveolar nerve. Soft tissue contour is determined by the presence of the underlying bone; and therefore anterior bone augmentation may be required from an aesthetic point of view. Egypt J Oral Maxillofac
c 2013 The Egyptian Association of Oral & Surg 4:16 Maxillofacial Surgeons. Egyptian Journal of Oral & Maxillofacial Surgery 2013, 4:16 Keywords: bone augmentation, implants, preprosthetic surgery Department of Oral and Maxillofacial Surgery, Barts Health Trust, Whipps Cross University Hospital, London Correspondence to Farah Aga, Department of Oral and Maxillofacial Surgery, Barts Health Trust, Whipps Cross University Hospital, London E11 1NR Tel: + 004 479 4840 1510; e-mail: farahaga@gmail.com Received 21 May 2012 accepted 20 July 2012

Bone and bone substitutes

Desirable properties of a bone substitute

Allografts

Bone is a composite material comprising collagen and hydroxyapatite. Bone may be cortical (such as load bearing bones), cancellous (such as vertebrae) or corticocancellous (such as the tibia). Greenwald et al. [1] stated that the ideal bone graft substitute is biocompatible, bioresorbable, osteogenic, osteoconductive, osteoinductive, structurally similar to bone, easy to use and cost-effective. Grafts should provide soft tissue coverage and be easy to obtain, cost-effective, stable, noninfective and resistant to resorption [2].

Allografts are resorbable processed bone grafts harvested from cadavers. Two common forms exist: freeze dried and demineralized freeze dried. Highlighted concerns with allografts as bone grafting materials include ease of sourcing, antigenicity and absence of absolute noninfectivity; however, an advantage is the elimination of an additional donor site surgical procedure, which may in turn reduce pain and morbidity [7].

Xenografts

Types of bone substitutes

To be stable, dental implants require a sufficient amount of bone surrounding them. The types of bone used for augmentation may include one or more of the following: autograft (from another site in the same individual, e.g. ramus, iliac crest), allograft (from one individual to another within the same species, e.g. interpore), xenograft (from a different species, e.g. BioOss) or alloplast (synthetically produced bone substitute material, e.g. Cerasorb).

Autografts

Biotechnological advances have identified a variety of bone grafting materials that may assist the implant surgeon. The gold standard of bone grafting material is the autologous bone [3,4]. Nonetheless, there are some disadvantages with the use of such a bone, which include site morbidity, difficulty of sourcing and resorption [5]. Hallman and colleagues reported that there are two ways in which an autologous bone graft may function: first, by acting as a scaffold and subsequently being resorbed as new bone is formed; second, by revitalization in situ, provided that the grafting process is carried out quickly and gently. They cite Davis et al. [6] as stating that a vascular supply must be within 0.1 mm from the osteocytes in the graft for it to function.
c 2013 The Egyptian Association of Oral & Maxillofacial Surgeons 2090-097X

Xenografts are graft materials obtained from animals. The bone is processed to completely destroy the organic component. Mardas et al. [8] carried out a randomized controlled trial on 27 patients to compare radiographical bone changes found in bone augmented with bovine xenograft and synthetic bone substitute. Periapical radiographs showing alveolar bone-level changes were obtained at regular intervals. No statistically significant differences in the changes in alveolar bone levels were identified between the two groups. Mardas et al. [8] also cite a randomized controlled trial carried out by Nevins et al. [9] that demonstrated that alveolar ridge resorption after extraction of a tooth was much lesser in sockets in which a deproteinized bovine bone graft was placed compared with those that were simply allowed to heal in a normal manner.

Alloplasts

Alloplasts are synthetic bone materials including calcium phosphate hybrids or composites and bioactive glasses. They behave as a scaffold for new bony ingrowth. Calcium phosphate hybrids are usually either nonsetting pastes or cements. Calcium phosphates are always osteoconductive. Cements either resorb slower than pastes or do not resorb at all. The advantage of alloplasts is that a secondary operation is not required [10].
DOI: 10.1097/01.OMX.0000424008.74895.09

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2 Egyptian Journal of Oral & Maxillofacial Surgery 2013, Vol 4 No 1

Bone augmentation techniques

Donos et al. [11] carried out a systematic review to compare clinical outcomes (success and survival) of implants placed in pristine sites and those placed in areas treated with various lateral ridge augmentation procedures, namely ridge expansion, guided bone regeneration (GBR) or bone grafting. Unfortunately, they found no randomized controlled trials. Nonetheless, two of these studies involving a small number of patients showed similar survival rates between implants placed in pristine sites and those placed in sites augmented with GBR. One included study with a 12-month follow-up period found similar survival rates between implants placed in pristine sites and those placed in areas in which lateral bone augmentation had been carried out with an autogenous bone graft using a staged approach. Bone grafting can be carried out at the time of tooth extraction, before implant placement (staged approach), at the time of implant placement or during correction of deficient areas around implants, such as a fenestration (simultaneous approach). In addition, bone can be augmented horizontally or vertically. Common intraoral areas requiring augmentation include the maxillary sinus region and the alveolar ridge. In a meta-analysis of two randomized controlled trials, Esposito et al. [4] concluded that vertical augmentation in mandibles resulted in a higher rate of implant failure than did the use of short implants in the same region without augmentation. However, a similar comparison between horizontal augmentation and short implants resulted in no statistically significant differences. Incidences of complications appear to be higher when vertical augmentation is carried out. However, in their review, Esposito et al. [4] also identified two trials in which vertically augmented bone was positively preserved for up to 3 years after loading. Nonetheless, they state in their review that their conclusions are based on few trials with small or very small sample sizes and relatively short follow-ups, implying that results should be interpreted with some caution. Aghaloo and Moy [12] state that within the alveolar ridge augmentation technique, different surgical approaches have been identified and categorized, including GBR; onlay/veneer grafting; combinations of onlay, veneer, interpositional inlay grafting; distraction osteogenesis; ridge splitting; free and vascularized autografts for discontinuity defects; mandibular interpositional grafting; and socket preservation. Descriptions and analyses of some of the common techniques used to increase bone volume are outlined below.

material is required, as in the case of a fully edentulous patient. However, the use of iliac or calvarial bone grafting is a cause for major discomfort in patients during the immediate postoperative phase [1416]. Nonetheless, Mertens et al. [17] found that donor site morbidity and graft resorption rates were less in sites where a calvarial bone graft had been used as opposed to an iliac crest bone graft. Block grafts are normally fixed to the recipient bone site with titanium mini screws (which may or may not need to be removed at the time of implant placement) or resorbable screws. It is common to fill in the gaps between the block graft and recipient bone site with bone chips or a particulate graft. Chiapasco et al. [18] concluded from their comparative study on alveolar distraction osteogenesis and bone grafting to correct vertically deficient ridges that the reconstruction of vertical defects with an autologous bone graft harvested from the mandibular ramus seems to be a reliable and relatively safe procedure, although the risk for permanent neural complications and infection is not negligible. Another problem with block grafting can be dehiscence of the soft tissue covering the graft, due to overstretching when replaced, compromising a tension-free primary closure [19]. Nissan et al. [20] recommend the use of a block in the anterior maxilla if an increase of 3 mm in either width, height or both is required. This is for the graft to be appropriately rigid and stable. Inlay grafting involves surgically sectioning an area of the bone and sandwiching a graft layer in between. Keller [21] has described Le Fort I osteotomy and the interpositional bone graft procedure before implant placement [4] (Fig. 1).

Particulate graft
Particulate autologous bone can be collected using bone collectors or from milled or prepared autogenous block grafts [22]. Bone traps may also be used to retrieve bone while preparing a surgical site for an implant. Young et al. [22] stated that in this way sufficient quantities of bone can be saved to correct small osseous defects such as fenestrations and dehiscences. This subsequently can reduce the use of allogenic bone material and avoid

Fig. 1

Block graft (inlay, onlay or veneer graft)

Onlay block grafts are those that are placed directly over the defective bony area to increase the width and/or height. The dimensions of the harvested block graft should ideally conform to the size of the defect to be managed. Autologous block grafts may be harvested intraorally from the chin, mandibular ramus, maxillary tuberosity or mandibular torus [13]. Extraoral autogenous bone grafts may be harvested from the iliac crest or calvarium; this may be indicated if there is insufficient intraoral bone available or if a large amount of bone graft

Block grafting.

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Bone augmentation in implant dentistry Aga 3

Fig. 2

Particulate graft harvesting.

preparation of a second surgical site. A particulate graft may be added a few months before implant placement or at the time of implant placement itself. Jensen and Terheyden [19] found, in a systematic review of bone augmentation procedures and materials, that the use of block grafts seemed to yield more gain in ridge height and a greater reduction in the need for additional grafting procedures than the use of granular grafts. However, they also noted that the best graft material for use in sinus lifting by the transalveolar approach is a particulate autograft. Aloy-Prosper et al. [13] carried out a review of 11 studies in which particulate graft material was used. They found that the success rate of implants placed in the augmented areas ranged between 85.7 and 100%. They concluded that particulate grafts were effective in correcting localized defects of the alveolar process (Fig. 2).

applied to cover up defects. Similar results were found by Rocchietta et al. [30], cited by Retzepi and Donos [23]. Successful bone regeneration has also been observed when guided bone regeneration, alone or in combination with bone grafts, has been used either for placement of dental implants after ridge augmentation or simultaneously with the placement of implants [11,25]. However, Esposito et al. [4], as cited by Retzepi and Donos [23], concluded that there was a lack of randomized controlled trials with evidence supporting the claim that the application of guided bone regeneration for treatment of dehiscences or fenestrations around implants promoted implant survival and success rates. Greenstein et al. [31] stated that the use of bone decortication is common during guided bone regeneration procedures to allow progenitor cells easy access to a guided bone regeneration treated site and to facilitate prompt angiogenesis. Unfortunately, to date, there are no human trials on its effectiveness; only animal trials have been carried out, which seem to negatively imply that its usefulness may be limited in clinical practice (Fig. 3).

Addition of growth factors and platelet-rich plasma

Bone morphogenic proteins are present in bone naturally and activate its development. In a Cochrane review on horizontal and vertical bone augmentation techniques for dental implant treatment, Esposito et al. [4] mentioned that growth factors and platelet-rich plasma (PRP) can be used to stimulate bone formation; however, at present, there is a lack of substantial evidence to conclude their efficacy in increasing the survival or success rates when used in conjunction with implant placement. PRP is a concentrated autologous source of growth factors, including platelet-derived growth factor, transforming growth factor, vascular endothelial growth factor, insulin-like growth factor and other growth factors derived from platelets. Steigmann and Garg [32] cited a study carried out by Marx et al. [33], in which radiographic assessment and histomorphometry were carried out to compare bone maturity and density between patients with bony defects who had received autogenous graft material in addition to platelet-rich plasma and control patients who had solely received an autogenous graft. The results showed that the patients who had received PRP had a denser bone, which matured at a faster rate.

Guided bone regeneration and barrier membranes

GBR is a technique used to repair osseous defects. One of the major complications of bone grafting is bone resorption. The GBR technique involves the application of a membrane to the site, the purpose of which is to prevent the nonosteogenic cells from reaching the soft tissues, and subsequently enabling the osteogenic cells from the native bone to populate the bony wound [23]. The use of barrier membranes in combination with particulate grafts and implants to augment the alveolar ridge and obtain ideal positioning of implants is reported to be an effective procedure in both humans and experimental animals [2427]. The presence of dehiscences around implants already in position can be improved by the placement of barrier membranes with allografts. Disadvantages of membrane placement can include dehiscence of the soft tissues, plaque growth or exposure of the membrane itself, possibly resulting in removal of the membrane [27,28]. Jensen and Terheyden [19], citing Carpio et al. [29], found no difference in the use of resorbable or nonresorbable membranes in promoting bone regeneration and osseointegration when

Bone manipulation techniques

Distraction osteogenesis

The basic principles of distraction osteogenesis were developed by the Russian surgeon Ilizarov. Chin [34] first described the use of distraction osteogenesis as a way to increase alveolar bone volume before implant placement. It is a procedure in which a gradual, controlled displacement of a surgically prepared fracture is used to increase bone volume [4]. McAllister and Gaffaney [35] stated that in order for distraction osteogenesis to be carried out, a minimum of 67 mm of bone must remain above the vital anatomical structures, with at least a 4 mm vertical defect of sufficient length. There are several types of distractor devices. Esposito et al. [4], in their

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4 Egyptian Journal of Oral & Maxillofacial Surgery 2013, Vol 4 No 1

Fig. 3

Representation of particulate bone grafting with membrane (Courtesy of http://www.dentalimplantologycostarica.com/bone-grafts.html).

Cochrane review, found that distraction osteogenesis resulted in greater vertical bone augmentation than other techniques. A comparative study on distraction osteogenesis and autologous bone vertical augmentation in vertically deficient edentulous alveolar ridges was conducted by Chiapasco et al. [18]. Eight patients were treated using autologous grafts from the mandibular ramus, whereas nine were treated by distraction osteogenesis. The study revealed similar implant success and survival rates in both groups. In addition, these rates were comparable with the success rates of implants placed in native bone. One of the risks of distraction osteogenesis is fracture of the host bone or transport segment. Other complications that can occur during distraction osteogenesis include infection, bleeding, nerve injury, adjacent tooth damage and flap dehiscence [35]. Distraction osteogenesis is unsuitable for use on knife-edge ridges. Patient compliance can also be a problem.
Ridge splitting and expansion

investigated the effectiveness of the ridge splitting technique were identified. Combining the results, a total of 531 implants were placed, out of which 517 survived, giving an overall survival rate of 97.4%. However, as there are very few studies on this technique, it is not possible to accurately draw any definitive conclusion on the effectiveness of ridge splitting as a bone augmentation method. More well-designed in-depth studies in this area are indicated. A systematic review by Donos et al. [11] included four studies on the split osteotomy technique. Implant survival rates varied from 95.8 to 100%. The most frequent complication with this technique was found to be the fracturing of the buccal plate during ridge expansion.

Alternatives to bone augmentation

Short implants

This is a technique in which the alveolar ridge is longitudinally split and parted. The implant is then directly placed in the space created, with or without graft material. In a review of augmentation techniques carried out by Aghaloo and Moy [12], two studies that [36,37]

Shorter implants may be an alternative treatment option to vertical bone augmentation. Annibali et al. [38] analysed two randomized controlled trials and 14 observational studies. They concluded that shorter implants (defined as less those than 10 mm in length) appeared to be successful, with high survival rates and low complication rates, in atrophic alveolar ridges over a short-term mean period of 3.5 years. However, it is clear that longer-term

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Bone augmentation in implant dentistry Aga 5

Fig. 4

n Gil et al. [40] determined from a systematic review Gala that success of zygomatic implants varied between 82 and 100%; however, lowest success rates were observed in postcancer resection patients.
Mandibular nerve transposition

dio [41] have discussed the option Chrkanovic and Custo of moving the inferior alveolar nerve laterally from its canal to overcome the problem of lack of bony height in mandibular implants. However, this procedure carries the risk of nerve damage and sensory dysfunction of the lower lip and chin; thus, the patient must be clearly informed about the risks and alternative treatment options.
Representation of distraction osteogenesis. Courtesy of Dr Kaseyli (http://www.drkaseyli.com/distraction.shtml).

Conclusion
The clinician must make the appropriate selection of graft material and technique on the basis of the size, shape, and dimensions of the defect and its location in the mouth. Thus, it is important for the clinician to review the literature to understand which graft material and which surgical technique will provide the best reconstructed osseous ridge to successfully support dental implant placement and long-term function [12]. It would seem pertinent, for example, to use a bone trap device on a drill while preparing an area of the bone for implant placement. This is a simple way to collect autologous particulate bone without the need for a second surgical site. This can then be preserved and used, if necessary, at the time of implant placement to cover up dehiscences or fenestrations. From the evidence obtained from various studies, it is clear that the use of membranes is controversial. One important factor to consider as a practitioner is the cost of a membrane, particularly when there is a lack of substantial evidence to support its use. When comparing the use of block grafting or ridge splitting to gain horizontal bone volume, this study advocates the former for the simple reason that fracturing of the buccal bone can be quite problematic if it occurs while attempting to split the ridge unless the surgeon is experienced in this technique. Many of the bone augmentation procedures described above are quite complex. In many of the studies, these procedures were carried out by skilful experienced clinicians, under ideal circumstances, in ideal patients. In reality, however, this may not always be the case and often caution is needed when deciding whether to carry out a particular augmentation procedure. The most pertinent question to ask is whether the procedure is the best option for the patient and will it positively affect the outcome of their overall treatment and experience. This should be carefully weighed against the risk for any complication that may occur while performing the selected procedure. Treatment planning should be carried out on an individual basis and appropriately tailored to meet the patients specific requirements. Other factors, such as cost, patient medical history and compliance, may also influence treatment planning. This may imply occasional consideration of the alternatives to bone augmentation, which have also included been included in this paper (Figs 4 and 5).

Fig. 5

Ridge splitting and implant placement. Courtesy of Dental implant professional (http://ajouimplant.blogspot.co.uk/2010/12/gbr-ggtr-forseverely-resorbed-ridge.html).

randomized controlled trials with larger numbers of implants are required to validate these outcomes. In addition, when the vertical height of the bone is less, shorter implants can result in longer suprastructures and compromised aesthetics [18]; and therefore, vertical bone augmentation may be preferable.

Zygomatic implants

Zygomatic implants can be used in atrophic posterior maxillae, in which conventional implant placement may not always be possible, as a possible alternative to sinus lifting or vertical bone augmentation. Stella and n Gil et al. [40], describe a Wagner [39], as cited by Gala variant of the original Branemark method of placement positioning the implant in the sinus through a narrow slot, following the contour of the malar bone, and introducing the implant in the zygomatic process, subsequently avoiding fenestration of the maxillary sinus and creating a vertical emergence angle at the first molar position.

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6 Egyptian Journal of Oral & Maxillofacial Surgery 2013, Vol 4 No 1

Acknowledgements
Conflicts of interest

There are no conflicts of interest.

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