grafting of tooth extraction socket with inorganic … of tooth extracted.pdfgrafting of tooth...

10
Grafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative Histometric Study in Rats Romeu Felipe Elias Calixto, PhD,* Juliana Mazzonetto Teo ´ filo, PhD,† Luiz Guilherme Brentegani, PhD,‡ and Teresa Lu ´ cia Lamano-Carvalho, PhD‡ T ooth loss is frequently accompa- nied by a progressive alveolar bone absorption, a situation that triggers bone ridge atrophy and causes difficulty to the placement of conven- tional or implant-supported prosthe- ses, while osseointegrated implants can barely or not be installed at all. 1–4 Therefore, preservation of the alveolar process in areas of tooth loss and adoption of procedures that minimize bone loss or recuperate the desirable alveolar ridge dimensions are impor- tant goals in dental practice. Clinical situations as those de- scribed above benefit from the use of biomaterials that may substitute for lost bone or stimulate osteogenesis. The most predictable results for re- placement, reconstruction, or filling of bone defects are still obtained with the use of autogenous porous bone grafts, nevertheless, their shortcomings such as surgical morbidity of the donor source and limited availability of healthy graft material. The alternatives to autografts include homogenous (al- logenic) and heterogenous (xeno- genic) bone grafts, besides a variety of synthetic materials, each of them pre- senting specific chemical composi- tions and physical characteristics that are more adequate for particular applications. 1,5 The availability and low cost of bovine bone, allied to the adequate processing that minimizes the risks of infection transmission, have led Bra- zilian, Canadian, and European com- panies to produce bovine bone grafts for medical and dental applications. 1,6 Heterogenous inorganic bone graft consists of matrix fragments in which the organic components are removed, and the mineralized elements, consist- ing mainly of hydroxyapatite, attain an osteoconductive surface behavior. 1,4,7 A variety of synthetic materials has been used to fill bone defects; among them the bioactive glasses, which are silica-based, surface-active compounds with the ability to bond directly to bone and also exert an os- teoconductive property. 8 Although the studies on biomate- rials have progressed considerably, the great variability of clinical and exper- imental models has made it difficult to evaluate the results in order to define the best material for specific dental or medical employments. The purpose of the present study was to compare, by histologic and histometric analysis, the behavior of inorganic bovine bone and bioactive glass particles grafted in the rat alveolar socket immediately af- ter tooth extraction, as well as their interference with the alveolar bone healing. Carried out in the same ani- mal specie and in an identical experi- *Post-Graduate in Oral Rehabilitation, Dental School of Ribeira ˜ o Preto-USP; Ribeira ˜ o Preto, SP, Brazil. †Professor of Pathology; Claretiano University Center, Ceuclar, Batatais, SP, Brazil. ‡Professor, Department of Morphology, Stomatology and Physiology, Dental School of Ribeira ˜ o Preto-USP; Ribeira ˜o Preto, SP, Brazil. ISSN 1056-6163/07/01603-260 Implant Dentistry Volume 16 Number 3 Copyright © 2007 by Lippincott Williams & Wilkins DOI: 10.1097/ID.0b013e3180500b95 Purpose: To compare histo- metrically, in rats, the bone healing after grafting the incisor extraction sockets with inorganic bovine bone or bioactive glass particles. Material: The volume fraction of grafted materials and alveolar healing components was estimated in histo- logic images at the end of the second and ninth weeks postoperatively by a differential point-counting method. Results: Both materials were his- tologically observed partially filling the cervical alveolar third and, al- though evoking neither a foreign body reaction nor a persisting inflamma- tory response, delayed new bone for- mation in trial areas around their particles. By the second week, the delay in bone healing was more pro- nounced in the animals grafted with inorganic than in those grafted with bioactive glass, and an opposing re- sult was observed during a 9-week period. Conclusion: Both inorganic bo- vine bone and bioactive glass particles grafted in the incisor extraction sock- ets of rats delayed new bone forma- tion, and the degree of impairment resulted from a combination of factors such as type of material and phase of the reparation process. (Implant Dent 2007;16:260 –269) Key Words: inorganic bovine bone graft, bioactive glass, alveolar heal- ing, bone healing 260 GRAFTING OF TOOTH EXTRACTION SOCKET

Upload: duongtu

Post on 01-Apr-2018

231 views

Category:

Documents


3 download

TRANSCRIPT

Page 1: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

Grafting of Tooth Extraction Socket WithInorganic Bovine Bone or Bioactive Glass

Particles: Comparative HistometricStudy in Rats

Romeu Felipe Elias Calixto, PhD,* Juliana Mazzonetto Teofilo, PhD,† Luiz Guilherme Brentegani, PhD,‡and Teresa Lucia Lamano-Carvalho, PhD‡

Tooth loss is frequently accompa-nied by a progressive alveolarbone absorption, a situation that

triggers bone ridge atrophy and causesdifficulty to the placement of conven-tional or implant-supported prosthe-ses, while osseointegrated implantscan barely or not be installed at all.1–4

Therefore, preservation of the alveolarprocess in areas of tooth loss andadoption of procedures that minimizebone loss or recuperate the desirablealveolar ridge dimensions are impor-tant goals in dental practice.

Clinical situations as those de-scribed above benefit from the use ofbiomaterials that may substitute forlost bone or stimulate osteogenesis.The most predictable results for re-placement, reconstruction, or filling ofbone defects are still obtained with theuse of autogenous porous bone grafts,nevertheless, their shortcomings suchas surgical morbidity of the donorsource and limited availability ofhealthy graft material. The alternativesto autografts include homogenous (al-logenic) and heterogenous (xeno-genic) bone grafts, besides a variety ofsynthetic materials, each of them pre-senting specific chemical composi-tions and physical characteristics that

are more adequate for particularapplications.1,5

The availability and low cost ofbovine bone, allied to the adequateprocessing that minimizes the risks ofinfection transmission, have led Bra-zilian, Canadian, and European com-panies to produce bovine bone graftsfor medical and dental applications.1,6

Heterogenous inorganic bone graftconsists of matrix fragments in whichthe organic components are removed,and the mineralized elements, consist-ing mainly of hydroxyapatite, attain anosteoconductive surface behavior.1,4,7

A variety of synthetic materialshas been used to fill bone defects;among them the bioactive glasses,which are silica-based, surface-active

compounds with the ability to bonddirectly to bone and also exert an os-teoconductive property.8

Although the studies on biomate-rials have progressed considerably, thegreat variability of clinical and exper-imental models has made it difficult toevaluate the results in order to definethe best material for specific dental ormedical employments. The purpose ofthe present study was to compare, byhistologic and histometric analysis,the behavior of inorganic bovine boneand bioactive glass particles grafted inthe rat alveolar socket immediately af-ter tooth extraction, as well as theirinterference with the alveolar bonehealing. Carried out in the same ani-mal specie and in an identical experi-

*Post-Graduate in Oral Rehabilitation, Dental School ofRibeirao Preto-USP; Ribeirao Preto, SP, Brazil.†Professor of Pathology; Claretiano University Center, Ceuclar,Batatais, SP, Brazil.‡Professor, Department of Morphology, Stomatology andPhysiology, Dental School of Ribeirao Preto-USP; RibeiraoPreto, SP, Brazil.

ISSN 1056-6163/07/01603-260Implant DentistryVolume 16 • Number 3Copyright © 2007 by Lippincott Williams & Wilkins

DOI: 10.1097/ID.0b013e3180500b95

Purpose: To compare histo-metrically, in rats, the bone healingafter grafting the incisor extractionsockets with inorganic bovine boneor bioactive glass particles.

Material: The volume fraction ofgrafted materials and alveolar healingcomponents was estimated in histo-logic images at the end of the secondand ninth weeks postoperatively by adifferential point-counting method.

Results: Both materials were his-tologically observed partially fillingthe cervical alveolar third and, al-though evoking neither a foreign bodyreaction nor a persisting inflamma-tory response, delayed new bone for-mation in trial areas around theirparticles. By the second week, the

delay in bone healing was more pro-nounced in the animals grafted withinorganic than in those grafted withbioactive glass, and an opposing re-sult was observed during a 9-weekperiod.

Conclusion: Both inorganic bo-vine bone and bioactive glass particlesgrafted in the incisor extraction sock-ets of rats delayed new bone forma-tion, and the degree of impairmentresulted from a combination of factorssuch as type of material and phase ofthe reparation process. (Implant Dent2007;16:260–269)Key Words: inorganic bovine bonegraft, bioactive glass, alveolar heal-ing, bone healing

260 GRAFTING OF TOOTH EXTRACTION SOCKET

Page 2: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

mental model, the species-specific andamong receptor bones differences,which might make comparisons unvi-able, were reduced.

MATERIALS AND METHODS

Male Wistar rats (250 g initialbody weight) were anesthetized with2,2,2-tribromoethanol (25 mg/100 gbody weight intraperitoneally; Al-drich, Milwaukee, WI), and the upperright incisors were extracted. Immedi-ately after tooth extraction, the alveo-lar socket of some of the animals wasfilled with particles of either inorganiclyophilized bovine bone matrix (Gen-ox®, Genius®; Baumer, Sao Paulo,SP, Brazil; particles of 0.25–1.00mm in diameter) or bioactive glass(PerioGlas®; USBiomaterials Corp.,Jacksonville Beach, FL; particles of90–710 �m in diameter) mixed with aminimum volume of sterile saline andintroduced with the aid of flexiblepolyethylene cannula and embolus.The wounds in the control (non-grafted) and grafted animals were su-tured with mononylon 4-0 (Ethicon,Johnson & Johnson, Sao Jose dosCampos, SP, Brazil), and a single dose(0.2 mL per rat, intramuscularly) of apolyvalent veterinary antibiotic(Pentabiotico Veterinario; Wyeth, SaoBernardo do Campo, SP, Brazil) wasadministered. The rats were housed un-der a climate-controlled environment(12 hours light/12 hours dark; 22 �3°C) with free access to standard labo-ratory chow and tap water. All proce-dures were conducted in compliancewith ethical principles for animal re-search, as approved by institutionalguidelines (Protocol 04.1.669.53.4).

The animals were killed with anintraperitoneal overdose of sodiumpentobarbital 1, 2, 3, and 9 weekspostoperatively (n � 5 per group inthe 1 and 3-week groups, for histolog-ical analysis; n � 10 per group in the2 and 9-week groups, for histologicaland histometric analysis), and theheads were immersed in 10% formalinsolution for 48 hours. After fixation,the maxillae were dissected free, de-calcified, and processed for paraffinembedding. Semi-serial longitudinal6-�m-thick sections of the hemi-maxillae containing the alveolar sock-

ets were cut at 60-�m intervals andstained with hematoxylin and eosin.

Histometric Analysis

The degree of new bone formationinside the alveolar socket was esti-mated at the end of the second andninth postoperative weeks in the cer-vical alveolar third (where the graftedparticles were located), by a differen-tial point-counting method using anintegration eyepiece with 100 equidis-tant points. A total of 500 points werecounted in 5 histological sections peralveolus (final magnification �100),the percentage of points lying on theparticles, on the connective tissue oron bone trabeculae being proportionalto their volume density. The measureswere standardized in the grafted andnongrafted sockets to avoid interfer-ence of regional differences in the rateof bone healing. The healing process,which in this phase consists of a grad-ual replacement of connective tissueby bone trabeculae, was estimated bynew bone volume fraction (percentbone trabeculae relative to bone tra-beculae plus connective tissue). Thenonparametric Mann-Whitney andKruskal-Wallis tests (� � 0.05 for sta-tistical significance) were used to an-alyze differences among groups.

RESULTS

Both inorganic bone and bioactiveglass particles of irregular shape andvariable size were observed partiallyfilling the cervical third of the alveolarsockets (Figs. 1A and 2A), and theirpresence evoked neither a foreignbody reaction nor a persisting inflam-matory response.

In the animals grafted with inor-ganic bone (Fig. 1), by the end of thefirst week, an osteoid matrix formingfrom the inner surfaces of the alveolarwalls approached the particles of thematerial but did not establish a directcontact with their surface. By the sec-ond week, neoformed bone trabeculaewere in close contact with the surfaceof some particles, and in a few ofthem, narrow absorption lacunae filledby connective tissue were observed.By the third and ninth weeks, theamount and maturation of new bonetrabeculae interposed among the par-ticles progressed, and in some cases, a

close contact between them was no-ticed. The amount of particles present-ing larger absorption lacunae filled by

Fig. 1. Rat alveolar socket at 1 (A), 2 (B and C),and 9 (D) weeks after tooth extraction and graft-ing with inorganic bovine bone (IB) particles.Hematoxylin and eosin. Particles of irregularshape and variable size filling the cervical thirdof the alveolar socket (original magnification�50) (A). Neoformed bone trabeculae (bt) inter-posed among the grafted particles and, insome cases, in close contact with their surface(arrowheads) (original magnification �100) (B).Inorganic bovine bone particle exhibiting a nar-row absorption lacunae filled by connective tis-sue (empty arrow) (original magnification �100)(C). Inorganic bovine bone particle showingnew bone trabeculae in close contact with itssurface (filled arrows) and absorption lacunaefilled by mineralized bone surrounding medul-lary vascularized connective tissue (empty ar-row) (original magnification �200) (D).

IMPLANT DENTISTRY / VOLUME 16, NUMBER 3 2007 261

Page 3: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

connective tissue increased, and by theninth week, in a few particles, thickerabsorption lacunae filled by mineral-

ized bone trabeculae surrounding amedullary vascularized connective tis-sue were observed.

In the animals grafted with bioac-tive glass (Fig. 2), by the end of thefirst week, an osteoid matrix interpos-ing among the particles and occasion-ally in close contact with their surfacewas observed. By the second week,the particles were surrounded by min-eralized new bone trabeculae, and insome particles, narrow absorption la-cunae filled by connective tissue wereobserved, likewise in the inorganicbone grafted group. By the third andninth weeks, as the reparation osteo-genesis developed, the particles wereprogressively enclosed by an increas-ing amount of neoformed bone, whichin several cases was in close contactwith their surface. In some particles,the absorption lacunae were filled byconnective tissue with discrete areasof osteoid matrix.

The histometric analysis showedthat the volume fraction of inorganicbone particles filling the cervical thirdof the alveolar socket was similar tothat of bioactive glass particles in both2 and 9-week groups. The volumefraction of the cervical alveolar thirdoccupied by the materials was 50% to80% in the 2-week period and 50% to62% in the 9-week period (Fig. 3). The

histometric data also confirmed a pro-gressive new bone formation in thecervical alveolar third from the secondto the ninth week in both grafted andcontrol groups, although more discretein the bioactive glass group, andshowed that the presence of eitherinorganic bone or bioactive glass par-ticles impaired the alveolar bone heal-ing. In the 2-week period, the delay inbone healing was more pronounced inthe animals grafted with inorganic bonethan in those grafted with bioactiveglass, and in the 9-week period an op-posing situation was observed (Fig. 4).

DISCUSSION

In the present study, the differentphases of alveolar healing were recog-nized by histological examination ofthe sockets of control and grafted ratsfrom 1 to 9 weeks after tooth extrac-tion. The chronology of the healingprocess that follows tooth extractionhas been well established in humansand different animal species. Shortlyafter tooth extraction, due to the rup-ture of blood vessels from the apicalregion and periodontal ligament, thesocket is filled with blood, whichimmediately coagulates. Capillarysprouting and fibroblasts originatingfrom periodontal ligament remnants

G B B I G B B I 0

0 2

0 4

0 6

0 8

0 0 1

Mat

eria

l (%

)

s k e e w 2 s k e e w 9

) 5 (

) 6 ( ) 8 (

) 9 (

Fig. 3. Percent of inorganic bovine bone (IB) and bioactive glass (BG) particles (median andinterquartile intervals, number of animals in parenthesis) in the alveolar cervical third, 2 and 9weeks after grafting (Mann-Whitney statistical test). No statistically significant difference be-tween groups was attained at each experimental period.

Fig. 2. Rat alveolar socket at 1 (A and B), 2 (Cand D), and 9 (E) weeks after tooth extractionand grafting with bioactive glass (BG) particles.Hematoxylin and eosin. Particles of irregularshape and variable size filling the cervical thirdof the alveolar socket (original magnification�100) (A). Osteoid matrix in close contact witha particle surface (arrow) (original magnification�200) (B). Mineralized new bone trabeculae in-terposed among the particles and a particleshowing absorption lacunae filled by connec-tive tissue (empty arrow) (original magnification�50) (C). Neoformed bone trabeculae in closecontact with a particle surface (filled arrow)(original magnification �100) (D). Bioactiveglass particle exhibiting neoformed bone tra-beculae in close contact with its surface (filledarrow) and absorption lacunae filled by connec-tive tissue with as discrete area of osteoid matrix(empty arrow) (original magnification �200) (E).

262 GRAFTING OF TOOTH EXTRACTION SOCKET

Page 4: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

and surrounding tissues invade the co-agulum, and, as wound healingprogresses, the blood clot is graduallyabsorbed and replaced by immatureconnective (granulation) tissue, whichbecomes progressively denser at thesame time as the amount of inflamma-tory cells and blood vessels decreasesand osteoblasts become evident. Theosteoblasts initially synthesize an imma-ture bone matrix (osteoid) that is furthermineralized by calcium deposition ashydroxyapatite crystals. The alveolarbone neoformation takes place from theapical and lateral walls toward the cen-ter of the alveolus, and the healing pro-cess culminates with filling of the dentalsocket by trabecular bone.9–12

Although histologic analyses havesuggested that the rat alveolar healingis completed by the end of the thirdweek after tooth extraction,13 quantita-tive studies have shown a discrete butsignificant increase in bone neoforma-tion up to the sixth10 or eighth12 week.Nevertheless, it has been proved thatthe major proportion of bone forma-tion14 and maximum mineral bonedensity12 take place by the end of thesecond week. In the present study, thehistometric analysis of bone healingwas carried out at the end of the sec-ond and ninth weeks after tooth ex-

traction, thus comprising both theperiod of maximum new bone forma-tion and end of the healing process.

Histometric data in the presentstudy showed that similar volumefractions of the cervical alveolar sock-ets were occupied by inorganic boneor bioactive glass particles 2 and 9weeks after implantation. Moreover,the volume fraction of both materialswas only discretely smaller after the9-week period than after the 2-weekperiod. Despite an attempt to achieve amore profound implantation, due tothe curvature of the extraction socketand also probably to the pressure ex-erted by bleeding, the materials weresuperficially located. Moreover, de-spite an effort to standardize the graft-ing procedures, it was not possible todetermine the precise amount of par-ticles introduced in the socket, and,thus, a comparison between periodswas not possible. It is worth empha-sizing, however, the small variabilityobserved in the material volume den-sity both between animals and be-tween experimental groups.

Distinct biomaterials have properabsorption rates when grafted in bio-logical environments, due not only tothe particle size but also to their chem-ical nature. In the present study, ab-

sorption lacunae were observed onlyin a few particles of inorganic bone upto 9 weeks after implantation, con-firming the extremely slow absorptionrate of this grafting material.15–18 In arecent review of biomaterials for hu-man maxillary sinus augmentation, in-organic bone was considered to be anonabsorbable grafting material.19

Likewise, absorption lacunae initiallyfilled by connective tissue and subse-quently presenting areas of osteoidmatrix were observed only in somebioactive glass particles, suggestingthis as a slowly degradable material.There are reports of an almost completeabsorption of PerioGlas® particles 12weeks after grafting in standardizedbony defects produced in femoral con-dyles of rabbits20–21 and 24 weeks aftergrafting in mandibular defects in mon-keys.22 Particles of another type of bio-active glass (Biogran®; Orthovita,Malvern, PA; 300–355 �m in diameter)presented a significant absorption only25 weeks after grafting in mandibulardefects in monkeys.23 Reports suggest-ing a rather fast degradation and/or re-sorption of bioactive glass particles havebeen questioned.24

The biocompatibility, as well asthe osteointegrative and osteoconduc-tive properties attributed to inorganicbovine bone grafts18,25 were corrobo-rated in the present study, which alsoconfirmed that the material can delaybone healing. Experimental and clini-cal studies from the 1950s and 1960srecommended inorganic bone graftsfor correction of oral and craniofacialbone defects. This material, however,has been reported to elicit an intenseand persistent inflammatory reactionin the tooth extraction socket of rats,consequently delaying alveolar bonehealing.26,27

Bio-Oss® (Geistlich Pharma AG,Wolhusen, Switzerland) is a grafting in-organic bone chemically and structur-ally comparable to that used in thepresent study, and has been tested inmedical and dental clinics since the1990s with reports of biocompatibility,osseointegration, and osteoconductionproperties.18,25 Both clinical and histo-logical analyses in humans have sug-gested that this is a material adequate forfilling tooth extraction sockets,28 andcorrecting alveolar bone ridges29 andperiodontal osseous defects.30 Stavro-

Fig. 4. Percent of new bone trabeculae (median and interquartile intervals, number of animalsin parenthesis) in the alveolar cervical third of control (Cont) and treated rats grafted withinorganic bovine bone (IB) or bioactive glass (BG), 2 and 9 weeks after tooth extraction(Kruskal-Wallis statistical test). For each postsurgery period, different letters indicate statisti-cally significant differences among the groups; A � B� C; � � 0.01).

IMPLANT DENTISTRY / VOLUME 16, NUMBER 3 2007 263

Page 5: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

poulos et al,24 however, have empha-sized that most of the clinical reportsare descriptive and vague, lacking ap-propriate controls, and have warnedthat conclusions based merely on clin-ical and radiographic studies might beimprecise. Besides, although histo-metric studies of maxillary sinus aug-mentation15 and healing of extractionsocket16 in humans have suggestedthat the volume density of reparationbone is not negatively affected by Bio-Oss®, it is worth mentioning that bothstudies also lack appropriate (non-grafted) controls.

Experimental studies carried outon animals have shown that particlesof Bio-Oss® implanted subperioste-ally for alveolar ridge augmentationand heterotopically in the rat abdomi-nal muscle exhibited no osteoconduc-tive property and induced a foreignbody reaction in both cases.31 A pos-sible benefit of their use for correctionof calvaria bone defects in rats andmandibular bone defects in dogs hasalso been contested.24 A histometricstudy in rats also confirmed that graft-ing Bio-Oss® as an adjunct to guidedtissue regeneration arrests new boneformation in mandibular bone defects.

In the present study, although ex-hibiting biocompatibility as well as os-teoconductive and osteointegrativeproperties, the bioactive glass particlesgrafted in the alveolar socket impairedbone healing. It has been postulatedthat bioactive glass particles im-planted into organic tissues are trans-formed by a specific ion exchangeprocess responsible for their osteocon-ductive, osteointegrative, and osteo-stimulatory properties. Initially, asilica-rich gel layer is formed, uponwhich an in situ calcium phosphatelayer is gradually precipitated. Subse-quently, organic species are incorpo-rated into this bioactively developinglayer, and osteoblasts are attracted toform new bone attached to the parti-cles’ surface. At the same time, fis-sures and lacunae forming in theparticles enable osteoprogenitor cellsto enter within this protected spaceand differentiate into osteoblasts,which form new bone without anyconnection with bone tissue outsidethe particles; this unique response ofbioactive glass to biological tissues

and fluids has been called osteostimu-latory property.32–34

Clinical and radiographic investi-gations have suggested the efficacy ofbioactive glass particles, particularlyPerioGlas®, in the treatment of humanbone defects resulting from periodon-tal disease, cyst resection, or apicec-tomy, as well as in the maintenance ofalveolar bone ridge and recuperationof atrophic alveolar processes forplacement of osseointegrated im-plants.32,35–38 Some of the authors,however, have recognized the need forhistological analysis to support thesefindings, but histological and histo-metric assessment has not always con-firmed clinical expectations. In thisrespect, no significant difference wasobserved in the percent of healingbone in human extraction socketsfilled with bioactive glass compared tocontrol (unfilled) sockets.39 Moreover,only a small amount of reparationbone was detected by histologicalanalysis in human extraction sites 6months after grafting with bioactiveglass for the placement of osseointe-grated implant.40 Likewise, althoughthe clinical and radiographic resultswere encouraging, histological analysisrevealed that, as a periodontal graftingmaterial, bioactive glass has only a lim-ited regenerative capability.41,42

Despite the emphasized osteo-stimulatory property of bioactive glassin dental clinical practice, experimen-tal results are still controversial. Theeffectiveness of bioactive glass parti-cles in promoting a higher reparationosteogenesis as compared to unfilledbone defects or defects grafted withhydroxyapatite and tricalcium phos-phate has been attested by histologicalanalysis in monkey22 and dog33 man-dibular bone, as well as in monkeyperiodontal defects43 and dog toothextraction sockets.44 Histometric dataattested also the positive action ofPerioGlas® grafted in the extractionsocket, reversing the adverse effect ofosteoporosis on alveolar bone healingin female rats.45 In this study, how-ever, the presence of bioactive glassparticles inside the socket of normal(nonosteoporotic) females tended toimpair the bone healing process on along-term basis (9 weeks). Likewise,the deleterious long-term effect ofBiogran® arresting bone formation

when used as an adjunct to guidedtissue regeneration in rats mandibulardefects was reported.24

It has been suggested that the os-teoconductive and osteostimulatoryproperties of bioactive glass result inpart from the uniformity of the parti-cles within a narrow size range. It hasbeen assumed that in particles smallerthan 200 �m, resorption occurs toorapidly and may cause inflammation,and, conversely, particles larger than400 �m remain unreacted and are notresorbed, thus preventing new boneformation34; an ideal 300 –355-�msize range has been considered.33 As aconsequence, Biogran®, with particlesof a narrower size range (300–355�m) than PerioGlas® (90–710 �m),would be more favorable to the forma-tion of absorption lacunae and to os-teoblastic cell migration, resulting in amore prominent osteostimulatoryproperty. Nevertheless, a histometricstudy46 aiming to compare the effectsof both materials grafted in bone de-fects of rabbits showed more newbone formation in the animals graftedwith PerioGlas®, and, in contrast tothe manufacturer’s information, themean particle diameter was larger forBiogran® (ranging from 457.9 to1312.5 �m) than for PerioGlas®(ranging from 94.4 to 964.8 �m). Theauthors described absorption lacunaein both materials, more frequently inparticles of PerioGlas® (32%) than inparticles of Biogran® (16%) 12 weeksafter grafting.

The histometric data in the presentstudy revealed that inorganic bonegraft had a more pronounced deleteri-ous effect on alveolar bone healingthan bioactive glass particles duringthe 2-week period, although an oppo-site result was observed during the9-week period. It is possible that liber-ation of silica, calcium, and phospho-rous, which takes place during the firstdays after the contact of bioactive glassparticles with biological fluids and isresponsible for their osteostimulatoryproperty,20 may have partially compen-sated for the negative effect of the phys-ical presence of this material, preciselyat the time when migration, prolifera-tion, and differentiation of cells of theosteoblastic lineage take place.

To our knowledge, there is no re-port in the literature on the short-term

264 GRAFTING OF TOOTH EXTRACTION SOCKET

Page 6: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

effects of grafting bioactive glasscompared to inorganic bone on clini-cal or experimental bone defects.However, comparison of bioactiveglass and synthetic hydroxyapatite asgrafting materials seems to favor theformer both on a short-term and long-term basis.33 There is histometric evi-dence of a faster and higher reparationosteogenesis after grafting bioactiveglass in bone defects of rabbit femuras compared to grafting synthetic hy-droxyapatite (both materials with par-ticle size ranging from 100 to 300�m).20 Similar results were reported af-ter a long-term histological analysis ofmonkey mandibular defects grafted withBiogran® compared to defects graftedwith synthetic hydroxyapatite.23

The present result for the 9-weekperiod group corroborates the report ofSchmitt et al47 comparing the effect ofgrafting critical-sized defects in therabbit radius with inorganic bone(Bio-Oss®) or bioactive glass (Perio-Glas®). Histological and histometricanalysis carried out 4 and 8 weekslater showed that the amount of newbone was significantly greater in thedefects grafted with inorganic boneafter both experimental periods. Bio-Oss® appeared also to be more effec-tive than PerioGlas® when used as anadjunct to guided tissue regenerationin the rat mandibular bone defectmodel on a long-term basis.24 The rea-son why inorganic bone graft, whichpresents only an osteoconductiveproperty, can be less deleterious ormore effective than bioactive glass inthe long term, in case this result isconfirmed in other experimental mod-els, deserves further investigation.

CONCLUSIONS

Both inorganic bovine bone andbioactive glass particles grafted in theincisor extraction socket of rats, al-though biocompatible and capable ofosseointegration, delayed new boneformation. Histometric data showedthat the degree of impairment resultedfrom a combination of factors, such asthe type of material and phase of thereparation process. Although a directextrapolation to the clinical aspect isimproper, the present results reaffirmthe need for reflection about the use of

biomaterials to substitute lost bone orstimulate osteogenesis.

Disclosure

All authors claim to have no fi-nancial interest in any company or anyof the products mentioned in thisarticle.

ACKNOWLEDGMENTS

The authors thank techniciansEdna A. S. Moraes, Antonio de Cam-pos, Adriana M. G. Silva e Gilberto A.Silva, for technical assistance. The au-thors also thank Genius-Baumer,which supplied the implant materials.Research supported by CNPq(300599/2003-0).

REFERENCES

1. Sanada JT, Canova GC, Cestari TM,et al. Histolic radiographic and immuno-globuline profile analysis after implantation ofblocks of demineralized bovine cancellousbone graft in muscle of rats. J Appl Oral Sci.2003;11:209-215.

2. Christensen GJ. Ridge preservation:Why not? J Am Dent Assoc. 1996;127:669-670.

3. Camargo PM, Lekovic V, WeinlaenderM, et al. Influence of bioactive glass onchanges in alveolar process dimensions afterexodontia. Oral Surg Oral Med Oral Pathol OralRadiol Endod. 2000;90:581-586.

4. Perri de Carvalho PS, Bassi APF,Pereira LAVD. Review and proposal of no-menclature for biomaterials. Implant News.2004;1:255-260.

5. Geiger M, Li RH, Friess W. Colla-gen sponges for bone regeneration withrhBMP-2. Adv Drug Deliv Rev. 2003;55:1613-1629.

6. Aichelmann-Reidy ME, Yukna RA.Bone replacement grafts: The bone substi-tutes. Dent Clin North Am. 1998;42:491-503.

7. Brunsvold MA, Mellonig JT. Bonegrafts and periodontal regeneration. Peri-odontol 2000. 1993;1:80-91.

8. Moore WR, Graves SE, Bain GI.Synthetic bone graft substitutes. ANZJ Surg. 2001;71:354-361.

9. Lin WL, McCulloch CA, Cho MI.Differentiation of periodontal ligament fi-broblasts into osteoblasts during sockethealing after tooth extraction in the rat.Anat Rec. 1994;240:492-506.

10. Lamano Carvalho TL, BrenteganiLG, Bombonato KF. Histometric analysisof rat alveolar wound healing. Braz Dent J.1997;8:9-12.

11. Devlin H. Early bone healing eventsfollowing rat molar tooth extraction. CellsTissues Organs. 2000;167:33-37.

12. Elsubeihi ES, Heersche JN. Quan-

titative assessment of post-extractionhealing and alveolar ridge remodeling ofthe mandible in female rats. Arch Oral Biol.2004;49:401-412.

13. Santos PV Jr, Melhado R. Effectsof ultrasonic stimulation on tooth extrac-tion wound healing: Histological study inrats. Rev Odontol UNESP. 1990;19:291-299.

14. Guglielmotti MB, Cabrini RL. Alve-olar wound healing and ridge remodelingafter tooth extraction in the rat: A histo-logic, radiographic, and histometric study.J Oral Maxillofac Surg. 1985;43:359-364.

15. Valentın P, Abensur D, Densari D,et al. Histological evaluation of Bio-Oss in a2-stage sinus floor elevation and implanta-tion procedure. A human case report. ClinOral Implants Res. 1998;9:59-64.

16. Artzi Z, Tal H, Dayan D. Porousbovine bone mineral in healing of humanextraction sockets. Part 1: Histomorpho-metric evaluations at 9 months. J Peri-odontol. 2000;71:1015-1023.

17. Araujo MG, Carmagnola D,Berglundh T, et al. Orthodontic movementin bone defects augmented with Bio-Oss®. J Clin Periodontol. 2001;28:73-80.

18. Orsini G, Traini T, Scarano A, et al.Maxillary sinus augmentation with Bio-Oss(R) particles: A light, scanning, andtransmission electron microscopy study inman. J Biomed Mater Res B Appl Bio-mater. 2005;74:448-457.

19. Merkx MA, Maltha JC, StoelingaPJ. Assessment of the value of anorganicbone additives in sinus floor augmentation:A review of clinical reports. Int J Oral Max-illofac Surg. 2003;32:1-6.

20. Oonishi H, Kushitani S, YasukawaE, et al. Particulate bioglass compared withhydroxyapatite as a bone graft substitute.Clin Orthop Relat Res. 1997;334:316-325.

21. Chan C, Thompson I, Robinson P,et al. Evaluation of bioglass/dextran com-posite as a bone graft substitute. Int J OralMaxillofac Surg. 2002;31:73-77.

22. Cancian DC, Hochuli-Vieira E,Marcantonio RA, et al. Utilization of autog-enous bone, bioactive glasses, and cal-cium phosphate cement in surgicalmandibular bone defects in Cebus apellamonkeys. Int J Oral Maxillofac Implants.2004;19:73-79.

23. Cancian DC, Hochuli-Vieira E,Marcantonio RA, et al. Use of BioGran andCalcitite in bone defects: Histologic studyin monkeys (Cebus apella). Int J Oral Max-illofac Implants. 1999;14:859-864.

24. Stavropoulos A, Kostopoulos L,Nyengaard JR, et al. Deproteinized bovinebone (Bio-Oss) and bioactive glass (Biog-ran) arrest bone formation when used asan adjunct to guided tissue regeneration(GTR): An experimental study in the rat.J Clin Periodontol. 2003;30:636-643.

25. Cardaropoli G, Araujo M,Hayacibara R, et al. Healing of extractionsockets and surgically produced–

IMPLANT DENTISTRY / VOLUME 16, NUMBER 3 2007 265

Page 7: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

augmented and non-augmented–defectsin the alveolar ridge. An experimental studyin the dog. J Clin Periodontol. 2005;32:435-440.

26. Okamoto T, Okamoto R, AlvesRezende MCR, et al. Interference of theblood clot on granulation tissue formationafter tooth extraction. Histomorphologicalstudy in rats. Braz Dent J. 1994;5:85-92.

27. Okamoto T, Garcia IR Jr, Mori GG,et al. Implante heterogeno de osso anor-ganico ao nıvel do tecido conjuntivo sub-cutaneo de rato. Estudo microscopio.Innovations J. 1999;3:26-29.

28. Cauwels RG, Martens LC. The useof anorganic bovine bone to correct a re-sidual osseous defect after toothextrusion: Report of case. ASDC J DentChild. 1999;66:273-277.

29. Callan DP, Rohrer MD. Use ofbovine-derived hydroxyapatite in the treat-ment of edentulous ridge defects: A hu-man clinical and histologic case report.J Periodontol. 1993;64:575-582.

30. Mellonig JT. Human histologicevaluation of a bovine-derived bone xeno-graft in the treatment of periodontal osse-ous defects. Int J Periodontics RestorativeDent. 2000;20:19-29.

31. Pinholt EM, Bang G, Haanaes HR.Alveolar ridge augmentation in rats by Bio-Oss. Scand J Dent Res. 1991;99:154-161.

32. Low SB, King CJ, Krieger J. Anevaluation of bioactive ceramic in the treat-ment of periodontal osseous defects. Int JPeriodontics Restorative Dent. 1997;17:359-367.

33. Shapoff CA, Alexander DC, ClarkAE. Clinical use of a bioactive glass partic-ulate in the treatment of human osseousdefects. Compend Contin Educ Dent.1997;18:352-358.

34. Froum SJ, Weinberg MA, TarnowD. Comparison of bioactive glass syntheticbone graft particles and open debridementin the treatment of human periodontal de-fects. A clinical study. J Periodontol. 1998;69:698-709.

35. Han J, Meng H, Xu L. Clinical eval-uation of bioactive glass in the treatment ofperiodontal intrabony defects. ZhonghuaKou Qiang Yi Xue Za Zhi. 2002;37:225-227.

36. Sculean A, Barbe G, ChiantellaGC, et al. Clinical evaluation of an enamelmatrix protein derivative combined with abioactive glass for the treatment of in-trabony periodontal defects in humans.J Periodontol. 2002;73:401-408.

37. Froum S, Cho SC, Rosenberg E, etal. Histological comparison of healing ex-traction sockets implanted with bioactiveglass or demineralized freeze-dried boneallograft: A pilot study. J Periodontol.2002;73:94-102.

38. Norton MR, Wilson J. Dental im-plants placed in extraction sites implantedwith bioactive glass: Human histology andclinical outcome. Int J Oral Maxillofac Im-plants. 2002;17:249-257.

39. Nevins ML, Camelo M, Nevins M,et al. Human histologic evaluation of bioac-tive ceramic in the treatment of periodontalosseous defects. Int J Periodontics Re-storative Dent. 2000;20:458-467.

40. Sculean A, Windisch P, KeglevichT, et al. Clinical and histologic evaluation ofan enamel matrix protein derivative com-bined with a bioactive glass for the treat-ment of intrabony periodontal defects inhumans. Int J Periodontics RestorativeDent. 2005;25:139-147.

41. Schepers EJG, Ducheyne P. Bio-active glass particles of narrow size rangefor the treatment of oral bone defects: A

1–24 month experiment with several mate-rials and particle sizes and ranges. J OralRehabil. 1997;24:171-181.

42. Fetner AE, Hartingan MS, Low SB.Periodontal repair using PerioGlas in non-human primates: Clinical and histologicobservations. Compendium. 1994;15:932-935.

43. Wilson J, Clark AE, Hall M, et al.Tissue response to bioglass endosseousridge maintenance implants. J Oral Implan-tol. 1993;9:295-302.

44. Teofilo JM, Brentegani LG,Lamano-Carvalho TL. Bone healing in os-teoporotic female rats following intra-alveolar grafting of bioactive glass. ArchOral Biol. 2004;49:755-762.

45. Furusawa T, Mizunuma K,Yamashita S, et al. Investigation of earlybone formation using resorbable glass inthe rat mandible. Int J Oral Maxillofac Im-plants. 1998;13:672-676.

46. Wheeler DL, Stokes KE, HoellrichRG, et al. Effect of bioactive glass particlesize on osseous regeneration of cancel-lous defects. J Biomed Mater Res. 1998;41:527-533.

47. Schmitt JM, Buck DC, Joh S, et al.Comparison of porous bone mineral andbiologically active glass in critical-sized de-fects. J Periodontol. 1997;68:1043-1053.

Reprint requests and correspondence to:Teresa L. Lamano-Carvalho, PhDDepartamento de MorfologiaEstomatologia e FisiologiaFaculdade de Odontologia de RibeiraoPreto–USPAv. do Cafe S/N14040-904 Ribeirao Preto, SP, BrazilPhone: (16) 3602-4012E-mail: [email protected]

Abstract Translations

GERMAN / DEUTSCHAUTOREN: Romeu Felipe Elias Calixto, PhD, JulianaMazzonetto Teofilo, PhD, Luiz Guilherme Brentegani, PhD,Teresa Lucia Lamano-Carvalho, PhD. Schriftverkehr: Teresa L.Lamano Carvalho, PhD, Departamento de Morfologia, Estoma-tologia e Fisiologia, Faculdade de Odontologia de RibeiraoPreto – USP, Av. do Cafe S/N, 14040-904 Ribeirao Preto, SP,Brasilien Telefon: (16) 3602-4012. eMail: [email protected] von Zahnextraktionshohlen mit anorganischemRinderknochengewebe oder bioaktiven Glaspartikeln. Einevergleichende histometrische Studie an Ratten

ZUSSAMENFASSUNG: Zielsetzung: Die vorliegende Ar-beit zielte auf einen histometrischen Vergleich der Knochen-

heilung bei Ratten ab, nachdem die Extraktionshohlen derSchneidezahne mit anorganischem Rinderknochengewebeoder bioaktiven Glaspartikeln als Transplantatstoff gepfropftwurden. Materialien und Methoden: Die Volumenaufteilungder Transplantatmaterialien und der Komponenten zur Alveo-larheilung wurde in histologischen Aufnahmen zum Ende der2. und 9. Woche nach dem operativen Eingriff mittels Dif-ferentialpunktzahlmethodik geschatzt. Ergebnisse: Bei bei-den Materialien wurde histologisch festgestellt, dass sieteilweise die die zervikalen Alveloardritten ausfullen. Undobwohl sie dort weder Fremdkorperreaktionen noch fort-dauernde entzundliche Tendenzen hervorriefen, verlang-samten sie doch die Bildung neuen Knochengewebes in denVersuchsbereichen rund um die entsprechenden Partikel. In

266 GRAFTING OF TOOTH EXTRACTION SOCKET

Page 8: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

der zweiten Woche wurde eine verstarkte Verzogerung derKnochenheilung bei den Versuchstieren beobachtet, beidenen eine Transplantierung mit anorganischen Materialienvorgenommen wurde, gegenuber den Tieren, bei denen alsTransplantat bioaktives Glas eingesetzt wurde. Ein gegenteil-iges Ergebnis wurde nach einem Zeitraum von 9 Wochenbeobachtet. Schlussfolgerung: Sowohl das als Transplantatin die Extraktionshohlen der Schneidezahne eingebrachteanorganische Rinderknochengewebe als auch die bioaktivenGlaspartikel haben zu einer Verzogerung der Knochengeweb-sheilung gefuhrt. Dabei ergab sich das Ausmaß der Behinde-rung aus einer ganzen Kombination an Faktoren, so wiebeispielsweise die Art des Materials sowie die Dauer desWiederherstellungsprozesses.

SCHLUSSELWORTER: Anorganisches Transplantat ausRinderknochengewebe, bioaktives Glasmaterial, alveolarerHeilungsprozess, Knochengewebsheilung

SPANISH / ESPAÑOLAUTOR(ES): Romeu Felipe Elias Calixto, PhD, JulianaMazzonetto Teofilo, PhD, Luiz Guilherme Brentegani, PhD,Teresa Lucia Lamano-Carvalho, PhD. Correspondencia a:Teresa L. Lamano Carvalho, PhD, Departamento de Morfo-logia, Estomatologia e Fisiologia, Faculdade de Odontologiade Ribeirao Preto – USP, Av. do Cafe S/N, 14040-904 Ri-beirao Preto, SP, Brasil. Telefono: (16) 3602-4012. Correoelectronico: [email protected] de la cavidad de extraccion de un diente con huesobovino inorganico o partıculas bioactivas de vidrio. Estudiohistometrico comparativo en ratas

ABSTRACTO: Proposito: Comparar histometricamente, enratas, la curacion del hueso luego de injertar las cavidades deextraccion incisivas con hueso bovino inorganico o partıculasbioactivas de vidrio. Material y Metodos: Se estimo la frac-cion de volumen de los materiales injertados y los compo-nentes de la curacion alveolar en imagenes histologicas alfinal de la segunda y novena semana posteriores a la opera-cion a traves de un metodo diferencial de cuenta de puntos.Resultados: Se observo histologicamente a ambos materialesmientras llenaban parcialmente el tercer alveolo cervical y, apesar de que no crearon una reaccion contra un cuerpoextrano ni una respuesta inflamatoria persistente, retrasaronla formacion del nuevo hueso en lugares de prueba alrededorde sus partıculas. Al llegar a la segunda semana, el retraso enla curacion del hueso fue mas pronunciada en los animalesinjertados con hueso inorganico que con el vidrio bioactivo yse observo un resultado inverso en un perıodo de 9 semanas.Conclusion: Ambos, el hueso bovino inorganico y las par-tıculas bioactivas de vidrio injertados en la cavidad incisivade extraccion de ratas retrasaron la formacion del nuevohueso y el grado de deterioro resulto de una combinacion defactores tales como el tipo de material y la fase del proceso dereparacion.

PALABRAS CLAVES: injerto de huevo bovino inorganico,vidrio bioactivo, curacion alveolar, curacion del hueso

PORTUGUESE / PORTUGUÊSAUTOR(ES): Romeu Felipe Elias Calixto, PhD, JulianaMazzonetto Teofilo, PhD, Luiz Guilherme Brentegani, PhD,Teresa Lucia Lamano-Carvalho, PhD. Correspondenciapara: Teresa L. Lamano Carvalho, PhD, Departamento deMorfologia, Estomatologia e Fisiologia, Faculdade de Od-ontologia de Ribeirao Preto – USP, Av. do Cafe S/N, 14040-904 Ribeirao Preto, SP, Brasil. Telephone: (16) 3602-4012,e-mail: [email protected] de alveolo de extracao dentaria com osso bovinoinorganico ou partıculas de vidro bioativo. Estudo com-parativo histometrico em ratos

RESUMO: Objetivo: Comparar histometricamente, em ratos,a cura do osso apos enxertar os alveolos de extracao deincisivos com osso bovino inorganico ou partıculas de vidrobioativo. Material e Metodos: A fracao de volume de mate-riais enxertados e componentes de cura alveolar foi estimadaem imagens histologicas no fim da 2a e 9a semana pos-operacao por um metodo de diferencial do contagem depontos. Resultados: Ambos os materiais foram observadoshistologicamente, preenchendo parcialmente o terco cervicale, embora nao evocando nem uma reacao a corpo estranhonem uma resposta inflamatoria persistente, atrasou a novaformacao de osso em areas de teste em torno de suas partıcu-las. Por volta da 2a semana, o atraso na cura do osso foi maispronunciada nos animais enxertados com inorganico do quenaqueles enxertados com vidro bioativo e um resultado postofoi observado num perıodo de 9 semanas. Conclusao: Tantoo osso bovino inorganico quanto as partıculas de vidro bio-ativo enxertados nos alveolos de extracao dos incisivos deratos atrasaram a nova formacao de osso, e o grau de prejuızoresultou de uma combinacao de fatores, tais como tipo dematerial e fase do processo de reparacao.

PALAVRAS-CHAVE: enxerto de osso bovino inorganico,vidro bioativo, cura alveolar, cura do osso

RUSSIAN /������: Romeu Felipe Elias Calixto, ��������������, Juliana Mazzonetto Teófilo, ��������������, Luiz Guilherme Brentegani, ��������������, Teresa Lúcia Lamano-Carvalho, ��������������. �������� ���: Teresa L. Lamano Car-valho, PhD, Departamento de Morfologia, Estomatologia eFisiologia, Faculdade de Odontologia de Ribeirão Preto –USP, Av. do Café S/N, 14040–904 Ribeirão Preto, SP, Brasil ������: (16) 3602-4012, ��� ��. �����:[email protected]

IMPLANT DENTISTRY / VOLUME 16, NUMBER 3 2007 267

Page 9: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

���� �� ����� �� ���� ��� ���� � ������ ������� � ����� ��� ��������� ������ �� �� ���.!�� ��� ��� ����� ���� �� ���� � ��� �������"

�#�$%#: & ��: ������ � ������������������������ ������ ��� � � ��� ������� � ������� ���� �������� ����� ������������� ����� ������� ������ ����� ��� � ��� ����� �������� ���� � ���. %�� ���� � � ���:������ � ���� ��� ��� ���� � ���� ��� ����������� ��� � �������� ����� �������� � �������������� ���� � � ����� 2-�� � 9-�� ��������� ��� ��� � �������� ����� �� ������������ . � ��������: �� � ���� � � ���� ��������������� �� � ������ � ������������� ����� ����� ������ �����; �� ���� � ���������� ��� ��� �� ���� � �� ������� �

�� ���� �� � ���� � �, ��� ��, � ���� � ���� ���� ������ �� �������� ��� ����� ������ �� �� � ��������� �� �� �. �� 2-�� ������ � ����� �� � ��� ���� ��� ����� ����� ��� ��� ���������, ������� ��� ��� �� ����� �������� ���� �, ��� � ���, ���� ��� ��� �� ��� ������������; � 9-�� ������ ������� � ��� ����������-���. �� �: � � ����� ����� � ����� ����, � � �

� ���� ��� �������� ���� , ��� ������ � ��-�� �������� ����� �������� ����� � ���,� ������ �� �������� ��� ����� ������ �� ��;����� ���� ���� � ���� �� ������ ��� � ���� ������, � � �� � ���� � � �� �� � ������������ .

'($)#��# !(���: ��� �� ����� ������������� ����, ��� ������� �����, � �������������, � � ��� ����

JAPANESE /

CHINESE /

268 GRAFTING OF TOOTH EXTRACTION SOCKET

Page 10: Grafting of Tooth Extraction Socket With Inorganic … of tooth extracted.pdfGrafting of Tooth Extraction Socket With Inorganic Bovine Bone or Bioactive Glass Particles: Comparative

KOREAN /

IMPLANT DENTISTRY / VOLUME 16, NUMBER 3 2007 269