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Revista Española de Cirugía Oral y Maxilofacial

On-line version ISSN 2173-9161Print version ISSN 1130-0558

Rev Esp Cirug Oral y Maxilofac vol.29 n.1 Barcelona Jan./Feb. 2007




Bone cavity filling with alloplastic material in maxillofacial surgery

Relleno de cavidades óseas en cirugía maxilofacial con materiales aloplásticos



S. Ochandiano Caicoya

Médico Adjunto. Servicio de Cirugía Oral y Maxilofacial. Hospital General Universitario Gregorio Marañón. Madrid, España

Dirección para correspondencia




Two types of defects are differentiated in bone regeneration studies. Those that lack a capacity for spontaneous regeneration during the entire life of the individual (critical size defect) and those that do have this capacity (non-critical size defect), providing the adequate conditions are found such as blood clot stability, space-maintaining and mechanical rest (the guided bone regeneration concept). In this controversy, bony defects of the maxillary sinus and the residual cavities after cyst removal are revised. Both are non-critical size defects that conserve several walls.
Many authors used to conclude that for sinus elevation, using autologous bone in the graft material was always necessary, either on its own or mixed differently with biomaterials in proportions that were not defined, 50:50, 20:80 etc. Clinical evidence, which has also been reflected in the literature over recent years, contradicts this conclusion and it has been stated that biomaterials on their own in the maxillary sinuses achieve results that are comparable to those achieved with autologous bone, providing the ossification period is increased. We review new studies that even dispute the need for using any type of graft at all in order to achieve new bone formation within the maxillary sinus.
The results in the residual cavities of bony defects after cyst removal, if various walls can be conserved, are even more conclusive. The best treatment for these defects is direct closure of the mucosa and waiting for the spontaneous regeneration of the defect. The use of autologous bone is unnecessary and, if we introduce biomaterials, we still do not achieve better biomechanical behavior of the residual bone. Ossification is delayed and the number of complications increases. Only in total thickness defects will the use of membranes be of any benefit.
The defects that have lost various walls can loose their capacity for spontaneous regeneration and, in these cases, autologous bone as well as biomaterials and regeneration membranes can be useful.

Key words: Bone regenerative; Alloplastic materials; Bone graft.


En los estudios de regeneración ósea se distinguen dos tipos de defectos, los que carecen de capacidad de regeneración espontánea durante toda la vida del individuo (defectos de tamaño crítico) y los que sí que poseen dicha capacidad (de tamaño no crítico), siempre que aportemos las condiciones adecuadas, estabilización del coágulo, mantenimiento del espacio y reposo mecánico (concepto de regeneración ósea guiada). En esta controversia revisamos el defecto óseo del seno maxilar y las cavidades residuales postquistectomía, ambos defectos de tamaño no crítico que conservan varias de sus paredes.
En la elevación de seno muchos autores concluían que era necesario aportar siempre hueso autólogo en el material de injerto, bien en solitario o en distintas mezclas con biomateriales en proporciones no definidas, 50:50, 20:80 etc. La evidencia clínica y la que recoge la literatura en los últimos años contradice esa conclusión y ya se afirma que los biomateriales en exclusiva en el seno maxilar consiguen resultados equiparables al hueso autólogo siempre que se aumente el periodo de osificación. Repasamos nuevos estudios que incluso discuten la necesidad de utilizar ningún tipo de injerto para conseguir neoformación ósea dentro del seno maxilar.
Los resultados en el defecto óseo de cavidades residuales postquistectomía, en las que consigamos mantener varias de sus paredes, son todavía más concluyentes. El mejor tratamiento de esos defectos es el cierre directo de la mucosa y esperar a la regeneración espontánea del defecto. La utilización de hueso autólogo es innecesaria y si aportamos biomateriales tampoco conseguimos un mejor comportamiento biomecánico del hueso residual, retrasamos la osificación y aumentamos el número de complicaciones. Sólo los defectos de espesor total pueden beneficiarse de la utilización de membranas.
Los defectos que han perdido varias paredes pueden perder su capacidad de regeneración éspontánea y en esos casos tienen utilidad tanto el hueso autólogo como los biomateriales y las membranas de regeneración.

Palabras clave:Regeneración ósea; Materiales aloplásicos; Injerto óseo.


"Bone substitutes may replace autogenous bone
for sinus lift procedures of extremely atrophic sinuses."
(Esposito M et al. The Cochrane Library Plus 2006. Number 2. Oxford)


Critical size and non-critical size defects

Bone reconstruction in an essential requirement for the complete functional rehabilitation of atrophic jaws and autologous bone is considered the "gold standard". However, there are very considerable inconveniences such as donor site morbidity and the limitation in the amount of bone available. In order to overcome these inconveniences the ideal bone substitute is tirelessly sought after.

The medical literature is full of papers searching for the ideal substitute for autologous bone. However, there are very common errors in methodology and in the interpretation of results that are repeated from one article to the next.

In order to obtain reliable clinical data on bone substitutes, we need suitable experimental animal models, and results that can be reproduced and compared.

The initial requirement for correct experimental models is that the bony defects should not heal spontaneously during the animal’s lifetime. These defects are known as critical size defects and they were initially described by Schmitz and Hollinger.1,2 Therefore, whatever defect that has the capacity to heal spontaneously is called a non-critical size defect. Convention established that if bone regeneration was not complete in the first 52 weeks, one could be certain that this would never occur.1,2

An example of an experimental model with a critical size defect could be the creation of circular defects with a total diameter thickness of 2 cm in the iliac crest, or square marginal mandibular defects of 5 cm in length, in 6 month-old mini-pigs weighing 10kg with removal in addition of the periosteum (Fig. 1). The pig is a good choice in these experiments, as its rate of bone regeneration (1.2-1,5 µm/day) is similar to that of humans (1.0-1.5 µm/day), and at 6 months they have completed their physiological growth.3

The regeneration of the critical size defect is difficult to achieve and it nearly always requires autologous bone. Normally in humans these are post-trauma defects, or defects caused by ablative oncological surgery. The immense majority of bony defects that we find in our daily clinical practice in oral, preprosthetic or implantological surgery are small or medium sized defects, that is to say NON-CRITICAL size defects.

At the beginning of this Controversy, we insisted on the concept critical size in order to establish clearly that the subject proposed always refers to non-critical size defects, which in this case are cavities, which are no more than defects that conserve various walls, as we shall see further ahead.

Bone regeneration in non-critical size defects has been widely studied under the concept of guided bone regeneration. Non-critical size defect has been defined as a bony defect that, under proper conditions, will heal spontaneously. These necessary bone conditions are the key to bone regeneration, and it is on this that the guided bone regeneration concept is based.

Guided bone regeneration implies providing suitable conditions so that the spontaneous and natural repair process of small sized defects can take place by means of new bone formation.

The conditions necessary for new bone formation are limited to:4

• Stabilization of the blood clot: micromovements in the blood clot that are above 10-20 µ sends mesenchymal cells towards fibroblasts and not towards osteoblasts.

• Maintaining the space or the dimensions of the defect: this is so that cellular and vascular invasion can take place together with proliferation.

• Functional rest: absence of mechanical load (difficult to achieve in orthopedic defects for example, but easy in the small defects of the jaw).4

As has been shown by Donos5 with calvarial bone in rats, what is most important is placing resorbable membranes, so that the space and stability of the blood clot are guaranteed, rather than placing material in the defect (Bio-oss® or enamel matrix proteins). In this revision we will only refer to non-critical size defects that follow the physiological sequence of guided bone regeneration. As we will see, if the conditions imposed for guided bone regeneration are followed, primary closure of the wound, or the placement of a simple membrane, will save us using not only autologous bone but also other types of bone substitute.


Bony defects of four or five walls. Non-critical size defect: residual cavities after cyst removal and sinus elevation

The subject of this Controversy is bone cavity filling with alloplastic material in the maxillofacial area. We are therefore discussing defects with a considerable capacity for spontaneous regeneration that we should make good use of. A mandible or maxilla that is undamaged is a structure that we can compare to a cube, and which therefore has six walls. Bone cavity refers to a bony defect within a wall. Depending on the number of walls containing the defect we refer to a five-wall defect (post-extraction socket when only the crestal wall is missing, which was occupied by the tooth), fourwall (residual cavity after cyst removal in which the vestibular and crestal walls are missing), three- or two-wall (presuming therefore that three or four walls have been lost respectively) and a one-wall defect (only basal bone is conserved).6

Post-extraction bony defects and post cyst removal defects are therefore defects of four or five walls, and the bony defect in the maxillary sinus can be considered also a defect of four or five walls. We are going to focus on the regeneration of residual cavities of cysts and on sinus elevation.

We have chosen sinus elevation because in this cavity ossification will take place providing a suitable blood clot has formed, the space is maintained and the collapse of the cavity is avoided. This is also the most used experimental model, where the greatest number of biomaterials have been tried and compared with autologous bone or compared with each other. In addition, it is a very predictable model and good results in nearly all materials are achieved providing the two necessary conditions mentioned are met. In general the osteogenic capacity of a material should be questioned if the clinical trials have been carried out in the maxillary sinus because, as we know, biomaterials only maintain the space and the blood clot in these defects, and they permit a process that would occur just the same if only, for example, a membrane or any other element for space maintenance were placed. As has been claimed by Glowacki, if we use biomaterials with non-critical defects we are only demonstrating the osteocompatibility of these materials, and not their osteoinduction.7,8

A certain question therefore immediately comes to mind: If these are defects that are going to regenerate spontaneously by themselves, under suitable conditions, why do we have to regenerate them with autologous bone, or with alloplastic material? Are we not interfering in a natural process that for example would occur just the same if a simple membrane were placed, or if direct closure were carried out?


Maxillary sinus elevation

The most predictable type of healing for oral bone is subantral vertical increase after sinus elevation,6 providing a suitable blood clot is achieved in the cavity that can be stabilized. It is for this reason that in the sinus elevation experimental model, different regeneration materials have been shown to work well, and excellent results have been obtained with autologous bone, demineralized lyophilized bone from human corpses, bovine hydroxyapatite with slow resorption, or even spontaneous ossification of the maxillary sinuses after trauma with a large intrasinus hematoma, which later then develops into ossification.9

The use of oxydized cellulose gauze (Surgicel®), which has no bone regeneration properties, but once placed under the antral membrane, it acts by maintaining the space and stabilizing the blood clot. The ossification mechanism is similar to that of the ossification of subperiostal hematomas in the long bones.10

A classical work of revision on sinus elevation was carried out by Merkx et al.11 in 2003. They analyzed the papers published on sinus floor augmentation with bovine hydroxyapatite, bioactive glass, hydroxyapatite and beta tricalcium phosphate, used on their own or mixed together in different proportions, or mixed with autologous bone or demineralized lyophilized heterologous bone. In order to include them in the revision, the studies had to have histomorphometric data. Among the conclusions the following stands out:

• The best material was autologous bone. There was a greater amount of new bone which was formed earlier (4 months). The main inconvenience was its resorption tendency after this period.

• Bovine hydroxyapatite is a material that is resorbed slowly with a bone density of 8-15% on re-entry. At six months it has this bone density that increases slowly over time given its slow resorption.

• Beta tricalcium phosphate is resorbed completely and at six months bone content is 30%.

• The ideal combination has not been established, or the best proportion of each of the mixtures.

The final conclusion of this study, which was a summary of many other previous studies, claims that using bovine hydroxyapatite on its own in sinus elevation should be avoided, and they advise that autologous bone and biomaterial should be mixed in different proportions, and if biomaterial is used as the only material for sinus elevation, they suggest the use of beta tricalcium phosphate.

That autologous bone needs to be one of the components of the mixture for success to be guaranteed, is something that has never been debated, and which has been recommended for many years. However, recently the metaanalysis in the Cochrane collaboration, directed by Esposito, affirms that even in very atrophic sinuses, biomaterial can be used on its own for sinus elevation with excellent results.12 This confirms what has been plainly visible in the literature over recent years.13,14

Hallman in 200215 and Szabó presented in 200516 two trials on sinus elevation with residual alveolar bone of less than 5 mm. Hallman15 studied three different sinus elevation groups. The first used autologous particulated bone from the mandibular ramus, and in the second group, bovine hydroxyapatite (Bio-Oss®) on its own with a resorbable membrane in the sinus window, and in the last group a mixture of 20:80 autologous bone/bovine hydroxyapatite was used. No differences were found among the groups with regard to clinical success or histomorphometry, and it was concluded that in very atrophic sinuses, biomaterial could be used on its own for augmentation, providing the ossification period was extended before placing the implants (9 months instead of 6).

Szabó16 presented a prospective multicenter study with bilateral sinus elevation of 20 patients with a residual alveolar ridge that was less than 5 mm. Using a split-mouth design, autologous bone was used on one side and beta tricalcium phosphate (Cerasorb®), on its own, on the contralateral side. Statistically significant differences were not found in the clinical success rate, radiological analysis or in the histomorphometry of the two groups and it was concluded that, in the experimental model for sinus elevation, beta tricalcium phosphate on its own is as useful as autologous bone.

Bruschi presented a new concept in 1998,17 which was the management or elevation in the maxillary sinus of just the sinus membrane (LMSF, localized management of the sinus floor), a concept that encompasses techniques for the fracture and surgical lifting of the maxillary sinus floor. This includes displacing the sinus membrane that is not perforated and in which a graft will not be placed. Implants, which will keep the membrane elevated, are placed in the same surgical act. The remaining alveolar ridge has a height of 5 to 7 mm. In this technique bone regeneration and osseointegration (97.5% success rate) occur simultaneously.

Winter 18 applied the same LMSF concept in 34 patients, but with an alveolar ridge height of less than 4mm. Implants were placed simultaneously and no implants of any type were used within the sinus. A success rate of 91.4% was obtained, and it was concluded that bone regeneration increases when a graft is not used which, as we know, always has to go through an initial period of resorption before new bone is deposited.

Lundgren,9,19 after observing spontaneous bone formation from a blood clot in the sinus after removal of a cyst,9 presented a study in 200419 in which they proposed sinus elevation by means of a lateral window. Filling material was not introduced and the membrane was elevated superiorly and sutured to the sinus wall. The bone window was replaced to ensure that the hematoma would fill the secluded space. Implants were simultaneously inserted in the residual alveolar ridge (the ridges had a height of between 4 and 10 mm), and primary stability of all implants was achieved. Osseointegration of all the implants was later achieved and, what was most important, ossification was observed at 12 months by CAT scan of the empty space, which had been occupied only by a hematoma within the window, membrane and residual ridge area. They concluded that there is a great potential for bone formation in the maxillary sinus without the need for grafts or any biomaterial, providing the principles of guided bone regeneration are followed. This is therefore a very novel study that should be given credit for applying bone regeneration concepts in a non-critical size defect, in which the space is maintained and the blood clot stabilized.

More recently Palma and Lündgren20 continued investigating the histological outcome of this empty, non-grafted space created in the maxillary sinus, and that is occupied post-elevation by a clot. In this study with primates, bilateral elevation of the sinuses is carried out with simultaneous placement of implants. On one side no grafting material of any kind was used. The membrane was raised, and kept raised, for the immediate insertion of the implants, while on the other side a graft of autologous bone was placed the conventional way. The bone window in the sinus wall was replaced so that a secluded space could be formed in the maxillary sinus that would permit bone regeneration. The height of the residual alveolar crest was some 3 mm, but in all cases primary stability of the implants was achieved and corroborated by resonance frequency analysis.

The results were striking. In the group with just membrane elevation they observed how, between Schneider’s membrane and the implant, there was bone forming, and how this extended around the implant in a vertical sense. In addition, osteogenesis was produced by apposition from the sinus walls, but there were also distant osteogenesis areas in the middle of the hematoma, away from the walls. Stability, measured by resonance frequency, increased in the membrane-elevated group, while in the autologous bone graft group, there was a reduction due to the resorption process of the graft to convert it into newly formed bone. In the sinuses with the bone grafts, necrotic looking bone in a remodeling process could be appreciated, together with bone particles surrounded by fibrosis. In the group with just membrane elevation, the new bone had a healthy appearance and there were areas of immature bone in transition to mature bone lamina with secondary osteomas.

For these authors the regeneration process in the group of just membrane elevation is a continuous bone deposition process as from the endogenous factors of the blood clot to the osteogenic mesenchymal cells contained in the membrane. This process, in the autologous bone group, starts with the resorption of grafted bone particles. They conclude that the mere elevation of the membrane and the maintaining of the space by the implants, results in the formation of bone and adequate osseointegration. The quantity of bone formed is no different from that obtained with autologous bone.20

Throughout the osteogenesis process within the maxillary sinus, we cannot forget the osteogenic potential of Schneider’s membrane, as has been demonstrated by Gruber21 in an experimental study with pigs. It is concluded that this membrane is a source of mesenchymal progenitor cells, and cells in the bone series that modulate their differentiation under the stimulation of morphogenetic proteins (BMP-6 and BMP-7).

As stated by Esposito,12 these preliminary results can appear surprising, and they suggest that wider multicenter trials should be carried out before recommending biomaterials instead of autologous bone as standard treatment for increasing extremely resorbed sinuses.

We would recommend, in view of the preliminary results obtained with membrane-elevation, to keep this elevated using mechanical methods (suturing or the presence of implants) and not to use any grafts. Many experimental and clinical studies are necessary before recommending this technique in a general way, but these are still spectacular results that arise in a very coherent manner from the guided bone regeneration concept for non-critical size defects (Fig. 2).


Residual cavities after cyst removal

This is an experimental model that has been studied considerably less than sinus elevation. However, everything that has been affirmed in sinus elevation is valid for cyst cavities, as these are nothing other than bony defects surrounded to a greater or lesser degree by walls. These are therefore non-critical defects with a great capacity for spontaneous regeneration.

It was thought that the advantage of bone regeneration with autologous bone or biomaterials was faster and more complete ossification with a view to earlier and more successful rehabilitation with, for example, osseointegrated implants,22 or minimizing the risk of fracture.23

The underlying idea in the literature is that a bone-based graft from the patient, or a bone substitute, not only reinforces the maxilla biomechanically, but it also increases the speed at which regeneration takes place.

Both conclusions are false. We know that autologous graft cells die when they are more than 100 µ away from a vascular source, (it has been calculated that 95% of a graft’s osteoblasts become necrotic) 24 becoming non-vital tissue, just as if bone substitute were used. Both materials should first be resorbed so that new bone can then be deposited in the zone. This process, consisting firstly of the active resorption of a non-vital and non-reactive tissue, followed by the apposition of newly formed bone, does not represent any advantage from the biomechanical point of view, and logically the regeneration period is delayed considerably.25

Chiapasco23 studied bone regeneration in 27 patients who underwent enucleation of mandibular cysts measuring more than 40 mm. No type of regeneration technique was used, and they just waited for spontaneous bone formation to occur. This was investigated by means of digital analysis of the density in panoramic radiographs and bone CAT scans. The parameters studied were the reduction of the cyst’s dimensions and the density of the newly formed bone. The conclusion at 24 months was clear and definitive. Complete and spontaneous bone regeneration occurred in all the cysts (despite their size) without the help of any bone filling material, which simplified the surgical procedure, reduced the risk of postoperative complications and costs.

The series that use grafts with a mixture of biomaterials and autologous bone, report a complication rate of 20% especially in larger cysts, with dehiscence of the surgical wound standing out, infection and extrusion of the graft material, all resulting in surgery in order to eliminate the graft material. This finally resulted in new bone formation that was slow and incomplete.26

Bodner27 compared cystic cavity regeneration by means of collagenous sponges (to maintain the space and for stabilization) and by means of lyophilized demineralized cadaver bone, without finding any statistically significant differences within both groups at two years.

Mitchell28 studied bone healing in cavities after cyst removal and two groups of 50 patients were analyzed. The control group showed spontaneous bone deposition while, in the test group, this occurred using a bovine collagen derivative. They demonstrated that bovine material, a strange body that should undergo degradation and be resorbed, considerably delayed ossification in the test group.

The use of different biomaterials has also been analyzed in other studies. The use of hydroxyapatite granules as well as bioactive glass has also resulted in increased complications (dehiscence, infection or granule extrusion). In addition hydroxyapatite requires active resorption by the receptor bed (with glass this is more like a non-active dissolution process) but very often this is incomplete, and the fibrous encapsulation of the granules can be observed, which results in only partial regeneration because of biomaterial persistence. 29,30

Guided bone regeneration by means of semipermeable membranes is also used in the regeneration of residual cystic cavities. In a controlled and randomized prospective study Santamaría, García, de Vicente, Landa and López Arranz,31 compared three groups of patients who underwent cyst enucleation. In the first group, only primary closure of the wound was carried out. In the second, the cavity was protected with a non-resorbable membrane, and in the third a resorbable membrane was used. Significantly different statistics were not found with regard to density and the volume of newly formed bone. This therefore demonstrates that the use of membranes does not improve bone formation in cystic cavities.

As claimed by Chiapasco,23 probably the only indication for using membranes in cystic cavities, is for total thickness defects, in which the vestibular cortical bone, as well as the lingual or palatal cortical bone, are destroyed as a result of expansion of the cyst (Fig. 3).



1. Bone cavities will always behave as non-critical size defects providing they conserve various walls. These defects have a great potential for spontaneous regeneration providing the blood clot is stabilized, the space is maintained, and the area is not subjected to mechanical load.

2. The maxillary sinus, as well as residual cavities following cyst removal, are defects of four or five walls of a non-critical size.

3. In sinus elevation the need for using autologous bone, or a mixture of bone and biomaterial so that predictable results can be obtained, is increasingly debated. Biomaterials on their own stabilize the blood clot and maintain the space leading to adequate ossification.

4. Preliminary studies suggest that the mere elevation of the membrane and maintaining the space using a well organized-blood clot, without placing any biomaterial, also produces correct osteogenesis. Prospective clinical and experimental and studies are necessary for obtaining definitive conclusions.

5. The treatment of choice for residual cavities following cyst excision with four or five wall defects, is direct closure and waiting for spontaneous regeneration to take place, except in total thickness defects (extensive destruction of both cortical structures) as only resorbable membranes for guided bone regeneration can be indicated.

6. Those residual cavities with adequate walls after cyst removal (for example where only one cortical structure has been lost, but not completely) using autologous bone grafts, mixtures of bone and biomaterial, or biomaterial on its own, will delay ossification. The biomechanical resistance of the defect will not improve, and complications increase.



Dirección para correspondencia:
Santiago Ochandiano Gaicoya
Pº de la Castellana, 100
28046 Madrid, España

Recibido: 31.10.06
Aceptado: 02.11.06



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