The International Journal of Periodontics & Restorative Dentistry © 2011 by QUINTESSENCE PUBLISHING CO, INC. PRINTING of TH

The International Journal of Periodontics & Restorative Dentistry

© 2011 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.. NO PART OF MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. 421

An Extraction Socket Classification Developed Using Analysis of Bone Type and Blood Supply to the Buccal Bone in Monkeys

Khalid Al-Hezaimi, BDS, MSc1/Paul Levi, DMD2/Robert Rudy, DMD3 In the past, the main concern for the Badar Al-Jandan, BDS, MSc4/Abdulaziz Al-Rasheed, BDS, MS5 clinician in implant dentistry was implant osseointegration. Today, with the understanding of bone remod- Bone modeling and remodeling following tooth extraction has been studied eling following tooth extraction and extensively. The reason for bone loss during the remodeling process is advancements in biotechnology multifactorial, and the primary reason for this loss is still yet to be determined. and biomaterials, the concerns are The aim of this study was to examine the type of bone and the blood supply to more related to postoperative com- the buccal bone in monkeys. Six maxillary arches from six monkeys were used. plications, function, and the final The arches were divided into three sections: right posterior, anterior from canine esthetic outcome.1–5 to canine, and left posterior. Blocks were decalcified and prepared for histologic Clinical and radiographic human processing and examination. Modified Masson trichrome and retic staining were and animal studies6–9 have shown used. Histologic sectioning demonstrated that the blood supply to the buccal that there is a loss of bone volume in bone came from the inner (socket) side of the alveolus, the periodontal ligament, the horizontal dimension of approxi- the adjacent interdental bone, and the supraperiosteal vessels emanating from mately 50% of the original width the covering gingiva or mucosa. Histologic examination showed that the buccal bone was composed of bundle and cortical bone. The thickness of the buccal of the alveolar bone that occurs bone was not uniform coronoapically, and the thinnest area of buccal bone was within the first 12 months postex- 6,10–15 the coronal portion. (Int J Periodontics Restorative Dent 2011;31:421–427.) traction. Such studies demonstrated that a marked diminution of 1Chairman and Assistant Professor, Eng.A.B. Research Chair for Growth Factors and Bone the height and width of the alveolar Regeneration, Division of Periodontology, College of Dentistry, King Saud University, Riyadh, ridge occurs following single or mul- Saudi Arabia. 2Associate Professor, School of Dental Medicine, Tufts University, Boston, Massachusetts, USA. tiple tooth extractions. The healing 3Associate Professor, Director of Predoctoral Periodontology, School of Dental Medicine, Tufts process following tooth removal University, Boston, Massachusetts, USA. results in greater resorption on the 4 Chair, Department of Biomedical Dental Sciences and Assistant Professor and Head of Oral buccal than on the lingual/palatal and Maxillofacial Surgery, College of Dentistry, University of Dammam, Dammam City, Saudi Arabia. aspects of the ridge. The reason this 5Assistant Professor, Eng.A.B. Research Chair for Growth Factors and Bone Regeneration, is important for postextraction ridge Division of Periodontology, College of Dentistry, King Saud University, Riyadh, Saudi Arabia. dimension alteration procedures is

that the buccal bone wall of an ex- Correspondence to: Dr Khalid Al-Hezaimi, Chairman Eng.A.B. Research Chair for Growth Factors and Bone Regeneration, PO Box 103851, Riyadh, 11616, Saudi Arabia; traction socket is comprised solely of fax: +966-1-4677854; email: [email protected]. bundle bone.10

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The bone remodeling phenom- Biopsy, histologic processing, enon has created recommenda- and analysis tions for the immediate placement of implants, suggesting that im- The animals were sacrificed with an mediate placement might prevent overdose of 3% sodium pentobar- bone resorption.16,17 It has been bital. Segments of the maxillae con- stated that the implant surfaces taining the anterior and posterior might help blood clot stability and teeth were removed en bloc along also help recruit osteogenic pro- with the adjacent teeth and alveolar genitor cells, which form bone in bone. The blocks were divided into direct contact with the implant.2–4 two segments: three anterior teeth Bone resorption is also affected by and the two premolars (right and the blood supply, implant surface, left). The blocks were fixed in a 10% presence of infection, and the pa- neutral formalin solution for 1 week. tient’s systemic health.18 They were decalcified in a solution of Araújo and Lindhe,10 in an ex- equal parts 50% formic acid and 20% periment in dogs, reported that sodium citrate for 10 weeks. The de- the first phase of extraction socket calcified specimens were washed healing is the complete resorption in running water, dehydrated, and of bundle bone (buccal bone) and embedded in paraffin. Buccolingual its replacement with woven bone. sections (7 µm) were obtained using Nevertheless, clinical observations a microtome with a diamond blade do not always follow this sequence, and stained using retic and modified where in many clinical cases, the Masson trichrome stains. ridge alteration following extraction is less than what has been suggest- ed in dog experimental models. Histomorphometric analysis The aims of the present study were to investigate the type of bone The histologic examination was and blood supply to the buccal bone performed using a light microscope in monkeys in vivo and to propose linked to a video camera/computer an extraction socket classification. (Buehler). The descriptive analysis of each histomorphometric param- eter in each monkey was done by Method and materials three examiners, each of whom evaluated the type of bone and Six monkeys (mean age, 3.4 years; blood supply to the buccal and in- mean weight, 32 Ib) were used in terdental bone. this study. The monkeys were used for internal medicine research and were then used for the present study after completion of the previ- ous project.

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BV CE GING CE

BB PDL CE PDL CB CB BuB SF BuB

IDB PDL BV

Fig 2 Photomicrograph of the interdental Fig 3 Photomicrograph of the buccal bone (IDB) in the mesiodistal direction show- bone in higher magnification showing the BV ing the large Haversian system (retic stain, thickness of the bundle bone adjacent to PDL magnification× 4). CE = cementum; BV = the blood vessel in the Haversian system blood vessel; PDL = periodontal ligament. (retic stain, magnification× 60). GING = gingiva; CB = cortical bone; BuB = bundle bone; PDL = periodontal ligament; D BV = blood vessel.

Fig 1 Photomicrograph showing the buccolingual section of a tooth with the surrounding buccal bone, which has a large Haversian blood vessel (retic stain, magnification ×4). BB = buccal bone; CB = cortical bone; BuB = bundle bone; PDL = periodontal ligament; CE = cementum; SF = Sharpey fibers; BV = blood vessel; D = dentin.

Results proportional to the volume of the buccal bone. Also, it was observed The histologic analyses showed that the bone covering these large that the blood supply to the buccal blood vessels from the socket side bone came from the inner (socket) of the alveolus was thinnest in the side of the alveolus, the periodon- coronal third of the socket (Fig 3). tal ligament (Fig 1), the adjacent The histology of these sections interdental bone (Figs 1 and 2), showed that the buccal bone com- and the supraperiosteal vessels prised both bundle and cortical emanating from the covering gin- bone (Fig 1). The bundle bone cov- giva or mucosa (Fig 1). It was found ered the inner aspect of the socket that the blood vessels that came wall, and lateral to the bundle bone from the adjacent interdental bone was the periodontal ligament, to the buccal bone were larger in which was attached to cementum diameter than the blood vessels in and identifiable (Fig 1). In addition the socket side of the alveolus from to the blood supply from the peri- the periodontal ligament. The pos- odontal ligament, there were large terior interdental bone blood sup- blood vessels that ran from the in- ply to the buccal bone was greater terdental bone and passed through than that of the anterior interden- the Haversian system in the cortical tal bone, and this appeared to be bone (Figs 4a and 4b).

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Fig 4a (left) Photomicrograph of the buccal BB (BB) and interdental bone (IDB) in the bucco lingual direction in higher magnification IDB showing the Haversian system within the bone trabeculae (magnification× 4).

Fig 4b (right) Higher magnification photo- BV micrograph of Fig 4a showing the Havarsian system and blood vessels running from the buccal to interdental bone. BV = blood vessel (magnification× 8).

The thickness of the buccal presence and thickness of the four bone was not uniform coronoapi- walls of the extraction socket. The cally, and the thinnest area of the classification of the extraction socket buccal bone was the coronal por- will help guide the clinician when im- tion. The Haversian system in the mediate implant placement is the coronal aspect of the buccal bone recommended choice. was adjacent to the thinnest portion of the buccal bone coronally • Class I: Extraction socket adja- and immediately adjacent to the cent to two non–periodontally bundle bone without any cortical involved natural teeth mesially bone present (Fig 3). and distally (Fig 5a) • Class II: Extraction socket adjacent to only one natural tooth Extraction socket classification either mesially or distally, where two contiguous non–periodon- The extraction socket classification tally involved teeth have been is based on the histologic finding extracted (Fig 5b) that the buccal bone has a blood • Class III: Extraction socket has supply from the adjacent interdental no immediate adjacent natural bone and not solely from the sock- tooth mesially or distally re- et side of the alveolus. For implant sulting from the extraction of placement immediately following three or more contiguous teeth extraction, the clinician needs to con- (Fig 5c) sider the periodontal biotype and the

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Fig 5 The extraction socket classification.

Fig 5a Class I: One extraction socket with Fig 5b Class II: Two extraction sockets Fig 5c Class III: Extraction socket(s) with adjacent natural teeth mesially and distally. with natural teeth on either side. no adjacent natural teeth.

Discussion trauma will occur during tooth ex- postextraction bone resorption re- traction, the bone of the socket side late to the significant blood sup- Bone remodeling following tooth of the alveolus is likely to be dam- ply of the interdental bone and the extraction has been well document- aged, and the blood vessels would presence of both bundle and corti- ed.6,8,10 Bundle bone is immature likely be severed or occluded. This cal bone. Partial bone resorption bone that contains thick bundles of may provide an additional explana- of the buccal and lingual socket collagen fibers arranged nearly par- tion for the complete resorption of walls will generally occur follow- allel to one another with osteocytes the buccal bone, not solely because ing tooth extraction and might be in between. A similar type of bone the vascularization of the buccal a result of the thinness of the coro- is found in regions penetrated by bone is supplied only by the peri- nal alveolar bone. In addition, the Sharpey fibers, which are associated odontal ligament. authors believe that the amount of with ligament and tendon attach- In a study in dogs, Cardaropoli resorption increases as the num- ments. This study showed that buc- et al19 demonstrated that most bun- ber of contiguous teeth extracted cal bone is not solely composed of dle bone resorbed in the 2 weeks increases because of the profound bundle bone and receives a signifi- following removal of the mandibu- loss of the interdental blood supply. cant blood supply from the adjacent lar premolars. The buccal bone When a single tooth is extracted interdental bone. The photomi- surrounding the premolar teeth atraumatically proximal to two non– crograph of a histologic specimen in dogs is very thin. In the current periodontally involved natural showed thin bundle bone in the in- monkey specimens, which have teeth, the bone resorption is usually ner coronal aspect of the alveolus similar bone and tooth anatomy less than that if two proximal teeth (Fig 1). There are blood vessels run- to humans, the buccal bone was are removed. If the two adjacent ning mesiodistally from the adjacent thicker and showed both bundle mesial and distal teeth are extract- interdental bone to the buccal bone and cortical bone. The authors feel ed, then the resorption will be at its (Figs 4a and 4b). Since it is likely that that the variable factors affecting highest level.

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Schenk20 demonstrated that a when the distance from the con- reduced blood supply may cause tact point to the alveolar bone crest the death of osteocytes and, as a was ≤ 5 mm, the papilla height was consequence, cause the necrosis of achieved predictably. This can be the surrounding mineralized tissue found in a single implant adjacent of the bony walls. This is in agree- to two non–periodontally compro- ment with the authors’ hypothesis mised natural teeth, similar to ad- for a classification of extraction jacent natural teeth.22–24 In addition, sockets based on the presence of the apico-coronal dimension has to adjacent interdental bone, which be ≤ 3 mm from the contact area for provides blood perfusion. The two proximal implants to achieve an greater the number of teeth ex- interdental papilla.21 Tarnow et al25 tracted, the greater the damage demonstrated that the minimum to the interdental bone, which re- distance between two proximal sults in a compromised blood sup- implants should be 3 mm to avoid ply to the buccal bone. Therefore, loss of peri-implant bone and, sub- the present histologic analyses sequently, apical migration of the demonstrate the presence of the gingival tissue. Therefore, Tarnow blood supply from the interdental et al21 concluded that the critical bone to the buccal bone in addi- factors for papilla adjacent to an tion to the supraperiosteal vessels. implant are the existence of healthy The authors feel that the bone and bone on the adjacent tooth and the soft tissue remodeling in a single location of this bone at a distance extraction socket adjacent to non– of ≤ 5 mm for a single implant or periodontally compromised teeth ≤ 3 mm between two implants. will be less than that if one or more When a single tooth is extracted, contiguous teeth are extracted ≤ 5 mm is needed for the papilla to because of a compromised blood fill the interdental space because of supply from the interdental bone to the height and blood supply of the the buccal bone. proximal attachment on the proxi- The current findings support mal tooth. the clinical observations of Tarnow The extraction socket classifi- et al21,22 regarding the height of the cation presented will help the prac- interdental papilla. The authors feel titioner to identify a situation where that the interdental bone blood an immediate implant placed in the supply is not only important for esthetic zone is predictable, rather bone resorption, or lack thereof, but than opting for delayed implant also relates to the soft tissue con- placement. The authors believe tours. Thus, both the blood supply that this new system will help the and the interimplant soft tissue con- clinician to communicate with their tour are, in part, proportional to the referring dentists and help explain number of contiguous teeth being to them and their patients the ra- extracted. As a result and as seen tionale for their clinical decision. in the studies by Tarnow et al,21,22

The International Journal of Periodontics & Restorative Dentistry

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