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Ridge preservation after tooth extrac- tion. Authors' affiliations: Ren E. Wang, Niklaus P. Lang, The University of. Hong Kong, Prince Philip Dental Hospital,.
Ren E. Wang Niklaus P. Lang

Ridge preservation after tooth extraction

Authors’ affiliations: Ren E. Wang, Niklaus P. Lang, The University of Hong Kong, Prince Philip Dental Hospital,

Key words: bone substitutes, GBR, implant dentistry, membrane, ridge preservation, tooth

Corresponding author: Prof. Niklaus P. Lang, DDS, MS, PhD, Dr, odont. hc.mult. The University of Hong Kong Faculty of Dentistry Prince Philip Dental Hospital, 34 Hospital Road, Sai Ying Pun, Hong Kong SAR PR China Tel.: +852 2859 0526 Fax: +852 2559 9013 Mobile: + 41 79 301 5505 e-mail: [email protected]

Abstract

Conflicts of interest: The authors declare no potential conflicts.

extraction

Background: Following tooth extraction, the alveolar ridge will undergo dimensional changes. This change may complicate the subsequent restorative procedure when oral implants are chosen. “Alveolar ridge preservation” has been assessed in various studies. Aim: To evaluate the more recent studies on this topic and to explore new insights under this topic. Material and methods: Animal studies and clinical studies have addressed different techniques. Results and conclusions: Implants placed into the fresh extraction sockets do not prevent the resorption of the alveolar bone. Simultaneous guided bone regeneration could partially resolve alveolar bone resorption. The use of root-formed implants does not preserve alveolar ridges. Moreover, various bone substitutes have been tested: magnesium-enriched hydroxyapatite, human demineralized bone matrix, and deproteinized bovine bone mineral have been shown to be effective in ridge preservation. Applying the guided bone regeneration principle using bone substitutes together with a collagen membrane has shown clear effects on preserving alveolar ridge height as well as ridge width. Soft tissue grafts or primary closure did not show beneficial effect on preserving the alveolar bone.

Date: Accepted 03 July 2012 To cite this article: Wang RE, Lang NP. New insights into ridge preservation after tooth extraction Clin. Oral Implants Res. 23(Suppl. 6), 2012, 147–156 doi: 10.1111/j.1600-0501.2012.02560.x

© 2012 John Wiley & Sons A/S

Following tooth extraction, the alveolar ridge will undergo structural changes. These changes in extraction sockets were amply demonstrated with histological observations in dog studies (Cardaropoli et al. 2003). At day 1 after extraction, the socket was occupied by a coagulum; this coagulum was comprised mainly of erythrocytes and platelets that were trapped in a fibrous matrix. Immediately adjacent to the hard tissue wall was the “bundle bone”, and principal fibers from periodontal ligament (Sharpey’s fibers) could be found invested in the bundle bone. These were also in direct contact with the coagulum. At day 3, the coagulum had been replaced by a richly vascularized granulation tissue. At day 7, newly formed blood vessels were evident in the primary matrix. Various types of leukocytes and collagen fibers had taken the place of the residual periodontal ligament as well as the granulation tissue. At day 14, most of the bundle bone had disappeared, and instead, adjacent to the newly formed blood vessels, “woven bone” started extending from the old bone of the socket walls toward the center of the socket. At day 30, woven bone underwent resorption, suggesting that the remodeling process had begun. At day 60, hard tissue

bridges separated the marginal mucosa from the socket, and bone marrow replaced woven bone at the center of the previous socket. At day 90, woven bone was replaced by lamellar bone. At days 120 and 180, most of the woven bone had been replaced by lamellar bone. The role of bundle bone in the dimensional change in the alveolar ridge was investigated in several dog studies (Arau`jo & Lindhe 2005; Arau`jo et al. 2005) At 1 week after extraction (Arau`jo & Lindhe 2005), the buccal bony crest was 0.3 mm coronal to the lingual bony crest, but at 2 weeks after extraction, the buccal crest became 0.3 mm apical to the lingual crest. This relative distance was increased to 0.9 and 1.9 mm at 4 and 8 weeks after extraction, respectively. It was also observed that the crestal region of the buccal bone wall was made up exclusively of bundle bone, whereas the corresponding region of the lingual bone was made of a combination of bundle bone and lamellar bone. Obviously, the function of bundle bone is to anchor the tooth in the alveolar bone through the invested periodontal ligament. As the tooth is extracted, the bundle bone will lose its function, and subsequently, will resorb. This may explain the more pronounced resorption of the buccal than the lingual bony crest.

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A recent systematic review evaluated the dimensional changes in the hard and soft tissues of the alveolar process up to 12 months following tooth extraction (Tan et al. 2012). It was concluded that after 3 months of healing, the horizontal resorption of the alveolar bone was 2.2 mm at the crest, and 1.3, 0.59, and 0.3 mm at 3, 6, and 9 mm apical to the crest, respectively; after 6 months of healing, the vertical resorption of the alveolar bone was 11–22%, whereas the horizontal resorption of the alveolar bone was 29 –63%. When soft tissue was included together with the hard tissue in the dimensional assessments at 3 months of healing, there was even an increase of 0.4 mm in the vertical dimension. At 12 months of healing, the vertical resorption of the alveolar ridge was 0.8 mm. Horizontally, the resorption of the soft and hard tissue together was 1.3mm and 5.1mm after 3 and 12 months of healing, respectively. This vertical as well as horizontal dimensional changes of the alveolar ridge may complicate the subsequent restorative procedures when dental implants are chosen. Over the past 20 years, increasing interest has arisen regarding a concept called “alveolar ridge preservation”, which was defined as “any procedure undertaken at the time of or following an extraction that is designed to minimize external resorption of the ridge and maximize bone formation within the socket” (Darby et al. 2008). As suggested by that review, studies promoting various techniques have been performed. Most of the studies included the measurements of dimensional changes of the alveolar ridge after a ridge preservation procedure. The purpose of this review was to evaluate these more recent studies and to explore new insights under this topic. Within the context of exploring new insights for ridge preservation, also studies of lower levels in the evidence hierarchy may be of interest to shed some light on the techniques designed to preserve the alveolar ridge after tooth extraction. These low evidence papers are generally case series that combine various protocols. However, this approach, should lead to clinical validation before recommendable for routine clinical application.

Animal studies Implants for ridge preservation Immediate implants alone

A decade ago, it was proposed that “early implantation may preserve the alveolar anat-

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omy and that the placement of a fixture in a fresh extraction socket may help to maintain the bony crest structure” (Paolantonio et al. 2001). However, this statement has been scrutinized later in a dog study (Arau`jo et al. 2005). In the right jaw of five dogs, implants were placed into the fresh extraction sockets, while in the left jaw, fresh sockets were left for spontaneous healing. After 3 months of healing, histological sections were obtained to assess the distance from the SLA level to the first bone-to-implant contact under microscope. On the buccal aspect, this distance was 2.6 mm at implant sites and 2.2 mm at the corresponding extraction socket sites. Hence, the immediate placement of dental implants clearly failed to prevent the resorption of the buccal bone walls. To further study the modeling of the buccal bony plate, the same group of researchers designed another dog study (Arau`jo et al. 2006). In that study, the implants were placed into the fresh extraction sockets in the right jaw and 2 months later, the same procedure was performed again in the left jaw. Following another 1 month, the dogs were sacrificed, and it was observed that after 1 month of healing, at the buccal aspect, good osseointegration had been achieved above the first thread of the implant. However, after 3 months of healing, the level of this osseointegration had receded to below the first thread as a result of the modeling of the buccal bone. In the molar regions, the degree of this modeling was much less compared with the premolar regions, most likely because of the wider original combined defect and bone wall dimensions in the molar regions. This study provided strong evidence for the continued modeling process of the buccal bony wall leading to buccal bone loss despite the good osseointegration that had already been achieved in early healing phases. Obviously, this phenomenon was less pronounced in sites with thicker buccal bony walls. Again, immediate implant installation failed to preserve the alveolar bone. In a study aimed at observing boneto-implant contact of orthodontic implants subjected to horizontal loading (Wehrbein et al. 1998), immediately placed implants with simultaneous horizontal loading achieved better osseointegration than those with delayed loading. Moreover, it was suggested in another dog study that “a static load may stimulate bone mineralization adjacent to titanium implants” (Gotfredsen et al. 2001). Finally, the hypothesis was tested whether or not immediate implant placement together with simultaneous loading

would help to preserve the buccal bone (Blanco et al. 2011). In a dog model, two implants were placed into the fresh extraction sockets at the premolar sites on each side of the mandible. At the time of the implantation, the implants on one side of the jaw received a prosthesis with occlusal contacts, while the implants on the other side remained unloaded during the whole experimental period. Three months later, the dogs were sacrificed. The histomorphometric results showed that the vertical distance from the implant shoulder to the first boneto-implant contact was on average 3.66 mm in the simultaneously loaded group and 4.11 mm in the unloaded group. This difference was not statistically significant, and hence it was concluded that “immediate implant placement with or without loading does not prevent bone resorption that occurs following tooth extraction.” Immediate implant with bone grafts

The effect of bone fillers (magnesiumenriched hydroxyapatite) on preservation of the alveolar bone around immediate implants was evaluated in a dog study (Caneva et al. 2011). Implants with a sandblasted acid etched surface (Zirti®, Sweden & Martina, Due Carrare, PD, Italy) were placed into the fresh extraction sockets bilaterally in the dogs’ jaws. The margin of the rough surface was placed at the level of the buccal bony crest. On one side of the jaw, the bone filler was applied into the gaps around the implants. The contralateral sites were left unfilled as controls. After 4 months of submerged healing, the dogs were sacrificed. Histomorphometric evaluations showed that the vertical distance from the junction between rough and smooth surface to the buccal bony crest was on average 0.7 mm in the group with the bone filler and 1.2 mm in the control group with no statistically significant differences between the groups. Obviously, the use of bone fillers around implants immediately placed into extraction sockets did not contribute significantly to the preservation of the buccal bone. In a recent experiment (Arau´jo et al. 2011), it has been demonstrated that the use of Bio-OssÒ collagen as a bone substitute filler in the space between the implant and the buccal bony wall resulted in the prevention of buccal soft tissue recession and a reduction in periimplant bone loss and allowed the buccal bone to be thicker at the marginal level. However, another similar animal study (Favero et al. 2012) was not able to confirm these differences in outcomes. © 2012 John Wiley & Sons A/S

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Immediate implant with GBR

In an AAP-commissioned review on bone augmentation techniques, it was recommended that immediate implant placement together with GBR techniques may yield outcomes comparable to delayed placed implants (McAllister & Haghighat 2007). Recently, a dog study was conducted to evaluate the influence of absorbable membranes on hard tissue alterations around the immediately placed implants (Caneva et al. 2010a,b,c). Implants with a rough surface (zirconium sandblasted acid etched) were placed immediately following extraction on both sides of the mandibles, on the test side of the jaw, collagen resorbable membranes were placed to cover the implants. On the control side of the jaw, the implants were left without membranes. After 4 months of intended submerged healing, all implants were found exposed to the oral cavity because of soft tissue dehiscences. The dogs were sacrificed and biopsies were obtained. The distance between the most coronal margin of the implant and the bone crest were measured. At the buccal aspect, this distance was 1.7 mm on the implants placed with GBR procedures, and 2.2 mm on the implants placed without GBR, and this difference was statistically significant. At the lingual aspect, this distance was 0.6 and 0.4 mm on the test sites and control sites, the difference not reaching statistical significance. There was no difference between the groups regarding the level of first bone-to-implant contact and the percentage of bone-to-implant contact. This study provided evidence that the use of collagen resorbable membranes at immediate implant sites contributed partially (23%) to the preservation of the buccal bony wall. Further studies of the same group of researchers (Caneva et al. 2011, 2012) explored the effect of GBR based on deproteinized bovine bone mineral on alveolar ridge preservation and the reparation of defects around osseointegrated implants. After hemi-sectioning the third mandibular premolars and extracting the distal roots, a recipient site was prepared for an implant. This was placed lingually, leaving a defect of about 0.6mm in width and 3mm in depth at the buccal aspect. While the other side of the jaw was used as control without GBR, deproteinized bovine bone mineral (DBBM) was place into the defects of the test site and covered with a collagen membrane. This treatment contributed to improved bone regeneration in the defects. However, regarding the buccal bony crest preservation only a © 2012 John Wiley & Sons A/S

limited contribution of DBBM particles was obtained (Caneva et al. 2011). In the second study on the same material the dimensional changes of the alveolar bony crest following the placement of DBBM particles into sockets immediately after tooth extraction, in conjunction of the placement of a collagen membrane, were addressed (Caneva et al. 2012). After 4 months of healing, no differences in soft tissue dimensions were found based on histological evaluations. Yet, the location of the soft tissue at the buccal aspect was more coronally at the test compared to the control sites. Hence, it was concluded that the application of DBBM concomitantly with the placement of a collagen membrane at implant sites placed in the socket immediately after tooth extraction contributed positively to the preservation of the alveolar process. In a similar study recently published (Park et al. 2011), immediate implants (Institute Straumann AG, Basel, Switzerland) were placed bilaterally in the dogs’ jaws in the premolar region. On the experimental side, a non-resorbable ePTFE membrane (Tefgen®, Lifecore Biomedical, Chaska, MN, USA) was placed on the buccal plate of the implant sites without coverage of the bone crest and was fixed with mini screws. In the control site, no membrane was placed. After 3 months of non-submerged healing, no membrane exposure occurred. The dogs were sacrificed and after histometric observation, the vertical distance from the rough and smooth surface interface to the buccal bone crest was on average 1.72 mm in the control group and 0.92 mm in the experimental group. This difference was statistically significant. Moreover, at the level 2 mm below the buccal bony crest, the mean thickness of the buccal bone walls was 0.4 mm in the control group and 1.49 mm in the test group. Again, this difference was statistically significant. From the above two animal studies, it appeared that the outcomes of using nonresorbable ePTFE membranes is superior to that achieved by resorbable collagen membranes. It should be realized that the techniques applied in the two studies were different. In the first study, the resorbable collagen membranes were placed on top of the implants without fixation, and primary closure was achieved at the completion of the surgery. However, during the healing period, all implants were exposed because of soft tissue dehiscences. In the later study, the non-resorbable membrane was placed on the buccal bone wall and fixed with mini screws to avoid membrane exposure. The mem-

branes were placed below the buccal bony crests, and no primary closure was intended, which meant that the flaps healed without tension. Consequently, membrane exposure was absent during healing. Shape of implants and implant positioning

Tapered or root-formed implants were designed to reduce the gaps around implants that were placed immediately into the fresh extraction sockets, thus filling the defect partially with titanium. The question arises if this type of implant design will help in preventing alveolar bone resorption around such implants. In a split-mouth design, mandibles of dogs received cylindrical implants 3.3 mm in diameter (Premium®, Sweden & Martina, Due Carrare, PD, Italy) immediately after tooth extraction (control) (Caneva et al. 2010c). A similar procedure was carried out with root-formed implants 5 mm in diameter (Kohno®, Sweden & Martina, Due Carrare, PD, Italy) on the test sites. After 4 months of non-submerged healing, the dogs were sacrificed and histomorphometric evaluations were performed. The mean vertical buccal bone resorption was significantly greater in the test group (2.7 mm) than in the control group (1.5 mm). In essence, the filling of gaps with root-formed implants failed to preserve the buccal bone. On the contrary, the bone resorption was more pronounced around the root-formed immediate implants that filled the extraction socket to a greater extent than did the cylindrical implants. The root-formed implants with a wider diameter occupied the entire socket, leaving no space between the implant and the buccal bony wall. In other words, the implant body was located closer to the outer surface of the buccal bony wall. Consequently, a greater portion of the implant was exposed in the supracrestal region after modeling and remodeling process, as the distance between the implant outline and the outer surface of the buccal bone appears to be a crucial factor for the preservation of the buccal bone. To evaluate the influence of implant positioning into extraction sockets on the maintenance of the buccal bone level (Caneva et al. 2010a), implants (Premium®, Sweden & Martina, Due Carrare, PD, Italy) were placed in the center of the sockets in control sites of mandibles, whereas in the test sites, the same implants were placed 0.8 mm deeper and more lingually. After 4 months of nonsubmerged healing, the histometric evaluations showed that the mean vertical distance from the rough and smooth surface interface to the buccal bone crest was significantly less

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in the test group (0.6 mm) compared with the control group (2 mm). Hence, the position of the implant had a greater impact on the preservation of the buccal bone resorption than the shape of the implant. Bone substitutes Bone substitutes alone

The effectiveness of ridge preservation with bone grafting in the extraction sockets alone was evaluated in a dog study (Boix et al. 2006). The maxillary and mandibular premolars were extracted. The sockets of the distal roots were filled with an injectable bone substitute (a polymer solution and granules of a biphasic calcium phosphate ceramic), and the sockets of the mesial roots were left unfilled as controls. Primary closure was achieved by overlapping hermetic sutures. After 3 months of healing, a tangent vector was drawn connecting the buccal and lingual crests, and the distance from the highest point of the alveolar ridge and this tangent vector was measured. There was a significant difference between the groups in the mandible (0.5mm and 0.4mm in test and control, respectively) and the maxilla ( 0.3 and 0.5 in the test and control, respectively). In another dog study (Shi et al. 2007), mandibular premolars and molars were extracted, the extraction sockets on the test side were treated with Surgical-Grade Calcium Sulfate (SGCS) + platelet-rich plasma (PRP) or with SGCS alone. On the control side, the sockets were left unfilled. Primary closure was achieved by periosteal releasing incisions and coronally advanced flaps. At baseline and 2 months after healing, CT scans were taken. Alveolar bone height was assessed on CT scans as the distance from the midpoint of the cortical bone to the inferior border of the mandible. It was found that the reduction in the ridge height was significantly greater in the control group compared with the test group (2.77, 1.39 mm, respectively), although no difference was found between SGCS + PRP treatment and SGCS treatment alone. In five beagle dogs (Fickl et al. 2008a,b), the 3rd and 4th mandibular premolars were extracted. In the test sites, the sockets were filled with Bio-Oss® collagen (Geistlich Biomaterials, W olhusen, LU, Switzerland). The collagen was fixed with sutures. The control sites were left untreated. After 4 months of healing, the histomorphometric evaluation documented a mean vertical buccal bone loss that was significantly lower in the test (2.8 mm) than in the control sites (3.2 mm). At 1 mm below the crest, the

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untreated group had a significantly narrower ridge width than the test group (3.7 mm vs. 4.4 mm). However, at 3 mm/5 mm below the crest, the ridge width was similar between the groups. Using digital image analysis on study casts for the same material (Fickl et al. 2008a,b) at the buccal aspect, the volumetric differences from baseline to after 4 months of healing was significantly greater in the control group (-2.2mm) than the test group (-1.5mm). These results showed small benefits toward using Bio-oss® collagen. A similarly designed study (Arau`jo & Lindhe 2009) compared sockets healing without treatment (control) and sockets treated with Bio-oss® collagen (test). Flaps were coronally replaced and primary closure was achieved in both types of sockets. After 6 months of healing, biopsies were obtained. Histometric analysis revealed that the dimensional changes in the apical and middle portion of the sockets were moderate in both sites, but in the coronal portion, the ridge width reduction was three times greater in the control sockets ( 35%) compared with the test sockets ( 12%). However, the composition between two sites was similar. The xenograft (Bio-Oss®, Geistlich Biomaterials, W olhusen LU, Switzerland)) only served as a scaffold and did not stimulate new bone formation. Another histometric study (Rothamel et al. 2008) compared sockets treated by Nanocrystalline hydroxyapatite paste (test) with unfiled sockets (control). Primary closure was achieved in both groups. After 3 and 6 months of healing, the dogs were sacrificed. Histometric analysis on lingual and buccal bone height, alveolar wall, and total bone width showed no difference for any parameters between groups. It could be concluded that Nanocrystalline hydroxyapatite paste does not appear to be effective for ridge preservation. Xenografts versus autografts

For many years, the use of autologous bone was regarded as a “gold standard” for augmentation procedures. To evaluate its efficacy in ridge preservation, a dog study was conducted (Arau`jo & Lindhe 2011). Extraction sockets in the mandibles of dogs were filled with either anorganic bovine bone or autogenous bone chips. After 3 months of healing, a histometric analysis was performed. The cross-sectional area of the ridge alteration was estimated by subtracting the cross-sectional ridge area identified after extraction from the corresponding area at the adjacent root. In the apical and middle portions of the sockets, no resorption was observed. However, in the

coronal portions, the ridge underwent resorption ( 25%) in the autogenous bone graft group. In the xenograft group, there was a positive change (3.6%). The residual grafting material was found to be 24.4%. Non-vital autogenous bone chips were found to be 1.9%. It seemed that autologous bone did not preserve the alveolar ridge. Primary flap closure Soft tissue grafts versus no soft tissue grafts

In five beagle dogs, the 3rd and 4th mandibular premolars were extracted (Fickl et al. 2008a). In the test group, the sockets were filled with Bio-oss® collagen, and free gingival grafts were obtained to cover the sockets. The control sites were also filled with Bio-oss® collagen (Geistlich Biomaterials, W olhusen, LU, Switzerland). The collagen was fixed with sutures, but no soft tissue grafts were applied. After 4 months of healing, the histomorphometric evaluation showed a mean vertical buccal bone loss that was significantly lower in the control group (2.8 mm) than in the test group (3.3 mm). At 1mm below the crest, the control group had significantly narrower ridge width than the test group (4.4 mm vs. 4.8 mm). But at 3 mm/5 mm below the crest, the ridge width was similar between the test and control groups. In another study digital image analysis on study casts from the same material (Fickl et al. 2008b), the remodeling process at the buccal aspect from baseline to after 4 months of healing was similar between the control and test groups ( 1.5 mm vs. 1.6 mm). These results, therefore, indicate the need for further human research using free gingival grafts to obtain primary closure for alveolar ridge preservation in well preserved alveoli.

Clinical trials Implants for ridge preservation Immediate implants alone

To observe the alteration of hard tissues following tooth extraction and immediate implant placement, a clinical study was conducted (Botticelli et al. 2004). In 18 patients, 21 SLA surface implants were placed. After 4 months of non-submerged healing without loading, a re-entry surgery was performed. The differences between the clinical measurements made before implant placement and after 4 months of healing yielded a horizontal resorption of the buccal bone of about 56%. The corresponding resorption of the lin© 2012 John Wiley & Sons A/S

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gual/palatal bone was 30%, whereas the vertical bone resorption was on average 0.3 mm at the buccal aspect and 0.6 mm at the lingual/palatal aspect. This amount of resorption is very similar with the resorption at human alveolar ridges after extraction reported recently in a systematic review (Tan et al. 2012). This, in turn, means that implants immediately placed into extraction sockets, also in humans, do not prevent the resorption of the alveolar bony ridge. Immediate implant with bone GBR

The effect of membrane placement in conjunction with or without bone substitutes for preserving the alveolar bony around implants immediately placed into extraction sockets of the anterior region (Chen et al. 2007) was studied in 30 patients that randomly received immediate implants (SLA surface, Institute Straumann AG, Basel, Switzerland) with Biooss® + collagen membrane (Geistlich Biomaterials, W olhusen, LU, Switzerland), Bio-oss® alone, or were left un-grafted. The dimensions of the alveolar bony crest were assessed at baseline and at the re-entry surgery after 6 months of healing. The implants were loaded after further 2 months, and the patients were followed up to 3 years after completion of restoration delivery. Standardized peri-apical radiographs and peri-implant examinations were performed every year. At the re-entry surgery, there was no significant difference between the groups on the vertical and horizontal defect reduction around the implants. On the other hand, the reduction in the horizontal distance from the outer surface of the buccal bony ridge to the implant surface was significantly greater in the control group (48.3 ± 9.5%) than in the bone graft alone group (15.8 ± 16.9%) and the bone graft with membrane group (20 ± 21.9%). During the 3-year post-restorative follow-up, all patients kept excellent oral hygiene. No difference was found regarding the periimplant or radiographic parameters between baseline and 1-year/3-year follow-ups or among the groups. This clinical study demonstrated that the bone defect around the immediately placed implants will heal predictably irrespective of the usage of membranes or bone grafts. However, the membrane or bone graft treatment may reduce the horizontal resorption of the buccal bony plate by 25% of the original dimension. Another clinical study was performed in the molar region, to examine the alteration of the alveolar bony ridge around implants immediately placed into molar extraction sockets after 6 months of healing (Matarasso © 2012 John Wiley & Sons A/S

et al. 2009); 12 immediate transmucosal implants with an sandblasted acid etched surface were placed in 12 patients. GBR was performed by placing a resorbable collagen membrane supported by a bone substitute (Bio-oss®). The alveolar bone dimensions around the implants were assessed at the time of implant surgery and at the re-entry surgery after 6 months of healing. The gaps around the implants healed as expected. However, the horizontal distance from the outer surface of the alveolar ridge to the implant surface at the buccal aspect was reduced by 58% on average. Unfortunately, no control group was provided in this study. An interesting aspect of this study was the influence of bone thickness on the buccal bone resorption. If the buccal bony wall was initially 1-mm thick, the buccal bone resorption was as high as 52%. However, when the buccal bone wall was initially 2-mm thick, the buccal bone resorption was significantly reduced to 33%. Shape of implants and implant positioning

As one of the proposed benefits of using rootformed implants was to avoid the need for bone augmentation, a multi-center randomized controlled clinical trial was conducted to test this hypothesis (Lang et al. 2007). In nine centers, 216 patients received either cylindrical or tapered implants (Institute Straumann AG, Basel, Switzerland) installed into the extraction sockets in non-molar regions. During the surgery, the type of implants was allocated at random and the need for guided bone regeneration was assessed. Whenever the gap around the implants was more than 0.5 mm or whenever buccal bony plate was thin (less than 1 mm), augmentation procedures were performed. Questionnaires were given to both patients and the operators to assess the preference to these two types of implants. The results revealed that 90% of both implant designs required GBR procedures. Patientreported outcomes did not show any preference toward any type of the implants. However, the surgeons’ perception was in favor of the tapered implants. Therefore, it is evident that root-formed implants do not offer an advantage in the need for avoiding GBR procedures. Another multi-center study aimed to a comparison of the dimensional bony changes around the two types of implants (Sanz et al. 2010). The hypothesis of the study was that, by providing more space for the coagulum around the implants, the cylindrical implants (test) should have a positive effect in preserving the alveolar bone and to reduce the hori-

zontal bone resorption by 20% when compared with the tapered implants (control). In three centers, 93 patients were included in the study. Forty-five cylindrical implants (Astra Tech AB, Mo¨lndal, Sweden) were installed into extraction sockets in the test group, and 48 tapered implants (Astra Tech AB, Mo¨lndal, Sweden) were placed in the control group. At baseline and at the re-entry surgery after 4 months healing, the results indicated that there was a marked reduction in the distance from the outer surface of the ridge to the implant in both groups (43% and 30%, respectively), although this difference was not statistically significant. Once again, it was evidenced that tapered implants cannot preserve the alveolar bony ridge. On the contrary, tapered implants were associated with more bone resorption. Non-surgical treatment Ultrasonic non-surgical treatment

The effect of ultrasonic application on bone healing has been studied in the orthopedic literature. In vitro experiments showed a significant influence of ultrasound on the proliferation of mandibular osteoblasts. Clinical evidence has also demonstrated that ultrasound treatment may accelerate the healing process of tibial diaphysis fractures by 38% in time (Kerr et al. 2008). In a randomized controlled split-mouth clinical trial, 12 patients who were scheduled for tooth extraction on both sides of the jaw were enrolled. At 7– 10 days following extraction, ultrasound therapy was delivered on the alveolar ridge of the test site for 20 min using a piezoelectric transducer for 10 sessions over the subsequent 4 weeks. Standardized cone-beam volumetric tomography (CBVT) scans were acquired at baseline (7–10 days post extraction), completion of ultrasound therapy (4 weeks after therapy), and 3 months post extraction. Dimensional changes of the buccal and lingual bony plates were analyzed through CBVT. However, given the limitations of small sample size and a short observational period with CBVT scans in this study, no significant differences could be found in absolute bony dimensional changes. Bone substitutes Bone fillers alone

In a randomized controlled clinical trial (Neiva et al. 2008), the effectiveness of an anorganic bovine-derived hydroxyapatite matrix delivered in a putty-form combined with a synthetic cell-binding peptide P-15

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(Putty P15) on ridge preservation was investigated. Comparisons were made between untreated control sockets and sockets treated with this putty-form matrix (test). Collagen dressing material was applied in both groups. After 4 months of healing, at the re-entry surgery, no difference was found between the groups in ridge width reduction ( 1.31 and 1.43mm in test and control, respectively). However, significantly less ridge height reduction was found in the test group (0.15 mm) compared with the control group ( 0.56 mm). The bone density assessed during implant surgery was found significantly higher in the test group as well. Another biomaterial, medical-grade calcium sulfate hemihydrates (MGCSH) was evaluated in a randomized controlled clinical trial (Aimetti et al. 2009). In the test group, 22 patients received this material in their sockets. As control group, 18 patients did not receive any treatment after extraction at all. Clinical measurements were performed at baseline and at the re-entry surgery (implant surgery). After 3 months of healing, significantly greater reduction in ridge height was found in the control group (1.2 mm) compared with test group (0.5 mm). Moreover, significantly greater ridge width reduction was found in the control group (3.2 mm) compared with the test group (2.0 mm). A histological analysis also found less lamellar bone and more woven bone in the control group. Two new materials were evaluated in a split-mouth clinical trial (Crespi et al. 2009). In 15 patients, three teeth were extracted in each patient. One of the sockets was treated with magnesium-enriched hydroxyapatite (Test 1). Another socket was treated with Calcium sulfate (Test 2). The third socket was left unfilled (control). The filling materials in the two test groups were secured with a collagen sheet covering and sutures to affix the membrane. Applying standardized intraoral radiographs obtained at baseline and 3 months later at the re-entry surgery, significant differences in ridge height reduction was found among all groups ( 0.48, 2.48, and 3.75 mm in the Test 1, Test 2, and control group, respectively). In histological analyses, the amount of vital bone was found to be significantly different among all groups (40.0, 45.0, and 32.8% in the Test 1, Test 2, and control group, respectively). The amount of connective tissue was not different between the test groups, but it was significantly different between the test and control groups. Significantly, less residual grafting material was found in sockets treated with Calcium sulfate. Based on this study, magne-

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sium-enriched hydroxyapatite was found to be more useful in alveolar ridge preservation than calcium sulfate. In a recent clinical split-mouth design study (Fernandes et al. 2011), sockets treated with anorganic bovine bone matrix (ABM) + synthetic cell-binding peptide P-15 (Test) were compared with unfiled sockets (control). The sockets in both groups were covered with Acellular dermal matrix (ADM). Clinical measurements were made at baseline and after 6 months of healing. No statistically significant differences could be found on ridge height reduction between the groups (1.5 and 1.2 mm in the control and test groups, respectively). But the ridge width resorption was significantly greater in the control (3.40 mm) compared with the test group (2.52 mm). The effectiveness of an allograft material in ridge preservation was recently tested in a randomized controlled clinical trial (Brownfield & Weltman 2012). Twenty patients were divided into two groups. The extraction sockets in the test group were treated with an allograft paste composed of “osteoinductive” demineralized bone matrix and cancellous bone chips, and the sockets in the control group were left unfilled. The sockets in both groups were covered with an absorbable collagen wound dressing. No significant difference on ridge resorption was found between the two groups as studied by CBCT/ Micro CT and histological analysis, although CBCT analysis found a significant correlation between initial buccal bony plate thickness and loss of ridge height. Different particle size

In general, smaller particles of bone substitutes are preferred because they may be resorbed more rapidly. They may enhance osteogenesis because of a greater surface area. On the other hand, the optimal particle size may depend on the bony defect to be grafted. Extraction sockets may benefit more using larger particles, as the sockets are usually larger than the periodontal defects. To elaborate on the most appropriate particle size to be used in extraction sockets, a randomized controlled clinical trial was conducted (Hoang & Mealey 2012) in 20 patients. One molar was extracted in each patient. The sockets were either filled with human demineralized bone matrix (DBM) putty with a single particle size (2–4 mm) or with multiple particle sizes (125–710 lm). Clinical assessments of the ridge dimensions were made at baseline and at re-entry surgery after 4–5 months of healing. No difference

was found on ridge width reduction between the single particle size group (1.4 mm) and multiple particle size group (1.3 mm). The vertical buccal and lingual bone loss was less than 0.5 mm in both groups. Histological analysis did not find any difference between the groups. Obviously, ridge preservation using this grafting material irrespective of its particle sizes was effective. Demineralized allografts versus mineralized allografts

Although both demineralized freeze-dried bone allograft (DFDBA) and mineralized freeze-dried bone allograft (FDBA) are claimed to be osteoconductive; only DFDBA has been proven to be osteoinductive. Both DFDBA and FDBA contain bone morphogenic proteins (BMP). As the process of demineralization facilitates the release of soluble factors like BMP, evidence suggested that a maximum of osteoinduction was observed when there was approximately 2% residual calcium in DFDBA. However, FDBA may serve as a superior scaffold compared with DFDB for space maintenance and may also be more osteoconductive. When osteoclasts break down the mineral content in FDBA until it is also demineralized, there could be a prolonged osteoinductive effect. To evaluate the clinical effectiveness of these two materials on ridge preservation, a randomized controlled clinical trial was performed (Wood & Mealey 2011). Forty patients were randomly allocated into two groups. The extraction sockets of the patients were filled with FDBA or DFDBA, respectively. All grafting materials were obtained from a single donor. Clinical measurements were performed at baseline and at re-entry surgery after 4–5 months of healing. No difference between the groups was found on ridge height reduction (1 mm in both groups) or ridge width reduction (2 mm in both groups). However, histological analysis yielded that the vital bone content was significantly higher in the DFDB group (38.42% vs. 24.63%), while the residual graft content was significantly lower in DFDBA group (8.88% vs. 25.42%). Although DFDBA may seem to be more osteoinductive, its effect on ridge preservation is similar to that of FDBA. Synthetic bone substitutes versus xenografts

Bone Ceramic® is a biphasic ceramic bone substitute. It is composed of a combination of hydroxyapatite (HA) and b-tricalcium phosphate (b-TCP). HA is insoluble. Although it is well tolerated in bone, its osteoconductive properties have been questioned. To be osteoconductive, the material should leave space for new bone to be depos© 2012 John Wiley & Sons A/S

Wang & Lang  Ridge preservation revisited

ited. Unlike HA, b-TCP is soluble. When it slowly resorbs, it is replaced by new bone. The objective of combining the insoluble HA with b-TCP, therefore, is that HA would maintain the space (scaffold function), while the b-TCP would resorb and promote new bone formation. A randomized controlled clinical trial was conducted to compare the ability of preserving alveolar ridges with this synthetic material (Bone Ceramic®,Institute Straumann AG, Basel, Switzerland) and a xenograft material, deproteinized bovine bone mineral (DBBM) (Mardas et al. 2010). Thirty patients were randomly assigned to two groups. One non-molar tooth in each patient was extracted, and the sockets in one group were filled with Bone Ceramic®, whereas in the other group, the sockets were filled with DBBM. A resorbable bi-layer collagen membrane was applied to cover each socket. Flaps were coronally advanced to close the wound as well as possible. Clinical assessments on ridge dimensions were made at baseline and at re-entry surgery after 8 months of healing. The reduction in the ridge width was significantly less in the Bone Ceramic® group ( 1.1 mm) than in DBBM group ( 2.1 mm). The reduction in the ridge height was negligible in both groups. Both materials partially preserved the width and interproximal bone height of the alveolar ridge. Bone Ceramic® achieved a better outcome in preserving the alveolar ridge. In a clinical study (De Coster et al. 2011), whereby bone regeneration in healing extraction sockets substituted with Bone CeramicÒ was compared with unfilled sockets, biopsies were obtained from the sites during later performed implant bed preparation. Healing was evaluated using transmitted light microscopy after 6–74 weeks (mean 22 weeks). 15 Bone ceramicÒ sites were compared with 10 naturally healed sockets. During implant placement it was clinically observed that bone at the substituted sites was softer than in control sites and large amount of loose biomaterial were found requiring thorough debridement. Consequently, some of the recipient beds were too large to get normal diameter implants initially stable. Hence, wider implants were necessary, and in 4 substituted sites, implants could not be installed at all. Additionally, it was reported that 2 out of ten implants installed in substituted sockets failed within 3 months after insertion. The histology showed that 5/ 15 substituted sites showed clearly incomplete healing. Overall, new bone formation was consistently poorer than in controls and presented with predominantly loose connective tissue and less woven bone. The grafting © 2012 John Wiley & Sons A/S

material appeared to interfere with the normal healing process. Hence, using this material for crestal bone preservation when implants are considered, even after long healing time, should be revised and based on additional scientific studies.

may increase in dimension to partially compensate the hard tissue resorption, especially in vertical direction. Hence, the assessment of study casts may not be appropriate to evaluate the effectiveness of ridge preservation procedures.

Collagen plugs

Guided Bone Regeneration (GBR)

Ideally, ridge preservation procedures should be easy and should not involve additional surgery. The use of collagen plug was introduced, as it has the mentioned advantages. To test its effectiveness on preserving alveolar ridges, a randomized controlled clinical trial was conducted (Kim et al. 2011). Twenty patients were divided into two groups. After the extraction of one molar in each patient, the sockets in one group were grafted with Bio-oss® and a collagen plug. Sutures were applied to fix the material. The sockets in the other group were left unfilled as controls. Study casts were obtained immediately at baseline and after 3 months of healing. Assessments of the bony height and ridge width were performed. After calculation, the average resorption rate of the bone height was 6.8% in the control group and 5.8% in the test group. There was no significant difference between the groups. The average resorption rate of the alveolar ridge width at 3 mm below the crest was 20.7% in the control group and 14.3% in the test group. Although this technique may be advantageous in preserving the alveolar ridge, no definite recommendations may be made. Collagen plugs with soft tissue grafts

To evaluate the effectiveness of a collagen plug together with soft tissue graft on ridge preservation (Oghli & Steveling 2010), 125 patients were divided into three groups. After tooth extraction, the sockets were treated with either a cone comprised of collagen (Test 1), a cone comprised of collagen and impregnated with gentamicin (Test 2), or left unfilled (control). In the two test groups, soft tissue grafts were harvested from the palate, and the sockets were covered with the sutured grafts. Study casts were obtained at baseline and after 3 months of healing. Assessments of the vertical dimension of the alveolar ridge were made on the casts. No difference was found among the three groups on vertical ridge resorption (0.8, 0.1, and 0.3 mm in Test 1, Test 2, and control groups, respectively). However, caution should be taken while interpreting these results. While using study casts to measure the ridge dimensions, soft and hard tissue alterations are included as indicated in a systematic review (Tan et al. 2012). Soft tissue

Ridge preservation with or without GBR

A cohort study was performed to follow 30 patients who received ridge preservation procedures with resorbable b-TCP of small particle size and resorbable collagen barriers after tooth extraction (Horowitz et al. 2009). Evaluating clinically the alveolar ridge width at baseline and at re-entry surgery 6 months later, a mean reduction in the ridge width of 12.4% was reported. Although there was no control group, it could be estimated from historical controls of a systematic review that reported on horizontal ridge resorption at 6 months after extraction (29–63%) (Tan et al. 2012) that this ridge preservation procedure applying the guided tissue regeneration principle was certainly effective. In a randomized controlled clinical trial (Barone et al. 2008), 40 patients were randomly allocated into two groups. After tooth extraction, the sockets of the patients in test group received guided bone regeneration procedures with cortico-cancellous porcine bone and collagen membranes. The sockets of the patients in the control group were left to heal spontaneously. Clinical measurements were performed at baseline and at re-entry surgery after 7 months of healing. It was found that the reduction in ridge width and height were significantly lower in the GBR group compared with control group (2.5 mm vs. 4.5 mm; 0.4 mm vs. 3 mm, respectively). Histological analysis revealed that the amount of cancellous bone was significantly greater in the GBR group (35.5% vs. 25.7%), and the amount of connective tissue was significantly less in the GBR group (36.6% vs. 59.1%). Membranes versus no membranes

To evaluate the adjunctive effect of resorbable collagen membranes to bone substitutes, a randomized clinical study was conducted (Brkovic et al. 2012). Twenty patients were randomly allocated into two groups. After tooth extraction, each socket was filled with a cone that is comprised of b-tricalcium phosphate (b-TCP) and type I collagen. The sockets in the test group were covered with collagen membranes, whereas the sockets in the control group were not. Primary closure was achieved in both groups by muco-perio-

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steal flaps. Clinical assessments were performed at baseline and at re-entry surgery after 9 months of healing. No statistical significant differences were found between the test and control groups on horizontal ridge resorption ( 0.86 mm vs. 1.29 mm, respectively) or on vertical dimensional changes (0.12 mm vs. 0.5 mm, respectively). Histometric analysis showed that there was no difference between the test and control groups regarding the amount of new bone (45.3% vs. 42.4%, respectively). Obviously, applying the cone material with or without membranes was effective in preserving the alveolar bone.







Primary flap closure Primary closure versus no primary closure

Primary closure can also be attained by means of an implant-supported provisional prostheses, or using a customized healing abutment. In a recent split-mouth clinical trial (Engler-Hamm et al. 2011), molars or premolars were extracted bilaterally in 11 patients. The sockets on both sides were filled with an inorganic bovine-derived hydroxyapatite matrix, cell-binding peptide P-15 (ABM/P-15), DFDBA, and covered with collagen membranes. Primary closure was achieved on one side (control). On the other side, the membranes were left uncovered (test). Clinical assessments of the ridge width were made using a caliper through a stent at baseline and at after 6 month of healing. In addition, questionnaires regarding the postoperative discomfort were filled by the patients. No significant differences were found on the ridge width changes (3 mm vs. 3.42 mm). However, the post-operative discomfort was significantly lower in the group without primary closure. The mucogingival junction was significantly more coronally displaced in the group with primary closure.

• •

Non-surgical treatment





Implants placed into the fresh extraction sockets do not prevent the resorption of the alveolar bone. Although osseointegration is achieved in the early stage (1 month in dogs), modeling of the bone may cause this level to recede apically.

There is not enough evidence to recommend ultrasonic instrumentation for alveolar ridge preservation and no conclusions on its clinical benefits can be made.

• •



Bone substitutes



• •

Although DFDBA may be claimed to be more osteoinductive, its effect on ridge preservation is similar to that of FDBA. A combination of hydroxyapatite and b-tricalcium phosphate (Bone Ceramic®) was twice as effective on preserving the alveolar ridge width when compared with deproteinized bovine bone mineral (Biooss®). However, the use of BoneCeramic® as a grafting material in fresh extraction sockets appears to interfere with normal healing processes of the alveolar bone, and hence its indication as a material for bone augmentation, when implant placement is considered, should be reconsidered (De Coster et al. 2011). Although collagen plugs were claimed to have an advantage in avoiding surgery, no definite recommendations can be made based on their poor outcome on preserving the alveolar ridge.

Guided bone regeneration



Applying the guided bone regeneration principle using bone substitutes together with a collagen membrane has shown clear effects on preserving alveolar ridge height as well as ridge width.

Primary flap closure





Conclusions Implants and associated techniques for alveolar ridge preservation

Immediate loading of the implants in dogs as well as in humans does not preserve the alveolar bone ridge. The use of bone fillers in residual defects around immediate implants placed in well preserved, intact alveoli in dogs may reduce soft tissue recession as well as vertical and horizontal resoprtion of the buccal bony plate. Simultaneous guided bone regeneration procedures could partially resolve alveolar bone resorption. However, this is depended on the type of membrane as well as the techniques applied. The use of root-formed implants, aiming at closing the space between the implant surface and alveolar bone of the extraction socket, does not preserve alveolar bone ridges. On the contrary, their use with this association was associated with accentuated bone resorption. It was demonstrated that thicker bony walls results in less resorption. The position of the implants was also an essential factor for the alveolar bone ridge preservation. Placing the immediate implant 0.8mm deeper and more lingually led to a reduction in the vertical buccal bone resorption by 70% in dogs after 4 months of healing.

A dog study revealed that using free gingival grafts in combination with bone substitutes did not provide additional effects on ridge preservation compared with bone substitutes alone. A clinical trial showed that achieving primary flap closure did not present additional beneficial effects on preserving the ridge width. On the other hand, patients experienced more discomfort with primary closed flaps. Moreover, the mucogingival junction was significantly more coronally displaced in the primary closed flap sites.

The only relevant dog study showed that unfilled sockets underwent three times the amount of horizontal resorption as sockets filled with xenograft (Bio-oss®). However, the xenograft only served as a scaffold and did not stimulate new bone formation. Various bone substitute materials have been tested in clinical trials for their effects on ridge preservation. Ridge preservation using human demineralized bone matrix was effective in ridge preservation irrespective of the particle sizes used, but allograft paste showed no effect.

Acknowledgements: This manuscript was supported by a grant of the Clinical Research Foundation (CRF) for the Promotion of Oral Health, Brienz, Switzerland. The senior author was an ITI Scholar 2010–2012 at the University of Hong Kong.

International Journal of Oral and Maxillofacial Implants 24: 902–909.

Arau`jo, M.G. & Lindhe, J. (2005). Dimensional ridge alterations following tooth extraction. An

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© 2012 John Wiley & Sons A/S