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University of Groningen Bone quality at the implant site after reconstruction of a local defect of the maxillary anterior ridge with chin bone or deproteinised cancellous bovine bone Meijndert, L.; Raghoebar, G.M.; Schüpbach, P.; Meijer, H.J.A.; Vissink, A. Published in: International Journal of Oral and Maxillofacial Surgery IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2005 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Meijndert, L., Raghoebar, G. M., Schüpbach, P., Meijer, H. J. A., & Vissink, A. (2005). Bone quality at the implant site after reconstruction of a local defect of the maxillary anterior ridge with chin bone or deproteinised cancellous bovine bone. International Journal of Oral and Maxillofacial Surgery, 34(8), 877- 884. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 17-03-2020

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Page 1: University of Groningen Bone quality at the implant site ... · isation of bone healing and remodelling. Several studies are available focusing on descriptive histology and histomorpho-metric

University of Groningen

Bone quality at the implant site after reconstruction of a local defect of the maxillary anteriorridge with chin bone or deproteinised cancellous bovine boneMeijndert, L.; Raghoebar, G.M.; Schüpbach, P.; Meijer, H.J.A.; Vissink, A.

Published in:International Journal of Oral and Maxillofacial Surgery

IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.

Document VersionPublisher's PDF, also known as Version of record

Publication date:2005

Link to publication in University of Groningen/UMCG research database

Citation for published version (APA):Meijndert, L., Raghoebar, G. M., Schüpbach, P., Meijer, H. J. A., & Vissink, A. (2005). Bone quality at theimplant site after reconstruction of a local defect of the maxillary anterior ridge with chin bone ordeproteinised cancellous bovine bone. International Journal of Oral and Maxillofacial Surgery, 34(8), 877-884.

CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).

Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.

Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.

Download date: 17-03-2020

Page 2: University of Groningen Bone quality at the implant site ... · isation of bone healing and remodelling. Several studies are available focusing on descriptive histology and histomorpho-metric

Clinical PaperPre-Implant Surgery

Bone quality at the implant siteafter reconstruction of a localdefect of the maxillary anteriorridge with chin bone ordeproteinised cancellous bovineboneL. Meijndert, G. M. Raghoebar, P. Schupbach, H. J. A. Meijer, A. Vissink: Bonequality at the implant site after reconstruction of a local defect of the maxillaryanterior ridge with chin bone or deproteinised cancellous bovine bone. Int. J. OralMaxillofac. Surg. 2005; 34: 877–884. # 2005 International Association of Oral andMaxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

L. Meijndert1, G. M. Raghoebar1,P. Schupbach2, H. J. A. Meijer1,3,A. Vissink1

1Department of Oral and MaxillofacialSurgery and Maxillofacial Prosthetics,University Medical Center Groningen andUniversity of Groningen, Groningen, TheNetherlands; 2University of Zurich, DentalInstitute, Department of Oral Microbiologyand General Immunology, Zurich,Switzerland; 3Department of Oral Function,Dental School, Faculty of Medical Sciences,University Medical Center Groningen andUniversity of Groningen, Groningen, TheNetherlands

Abstract. The purpose of this study was to investigate the quality of bone at graftedimplant sites in the anterior maxilla. Grafting of these sites was necessarybecause of insufficient bone volume in a buccopalatinal direction (width at the topof the crest 1–3 mm).Reconstruction was performed with chin bone (N = 5), chin bone and a resorbable

Bio-Gide1GBRmembrane (N = 5) or Bio-Oss1 spongiosa granules in combinationwith aBio-Gide1GBRmembrane (N = 5). Biopsieswere taken prior to implantation,i.e. 3months after graftingwith chin bone, and 6months after graftingwithBio-Oss1.Evaluation was done by assessing the histological and histomorphometriccharacteristics of full-length biopsies taken from the actual implant site.Both areas with non-vital bone and areas with apposition of bone and remodelling

phenomena were observed in the chin bone group at the time of placement of theimplants. Similar results were observed at implant sites reconstructed with achin bone graft covered by a membrane. In the chin bone group without and with aGBR membrane, the mean total bone volume (TBV) was 55.2 � 6.8% and57.7 � 11.5%, respectively; the marrow connective tissue volume (MCTV) was44.8 � 6.8% and 42.3 � 11.5%, respectively. Remnants of the resorbable GBRmembrane were not detected. In the Bio-Oss1 group, at implant placement somenewly formed bone was observed in the connective tissue surrounding theBio-Oss1 particles (mean TBV (newly formed bone) 17.6 � 14.5%), but mostparticles were surrounded by connective tissue. No convincing signs of remodellingwere observed (mean remaining Bio-Oss1 volume 40.5 � 9.3%; mean MCTV41.9 � 13.1%). No implants were lost during follow up (12 months).At the time of placement of the implants the grafting material (either chin

bone or Bio-Oss1) is still not fully replaced by new vital bone. In case of Bio-Oss1,most of the grafting material is even still present. Despite these differences,the 1-year clinical results were very good and comparable between the variousgrafting techniques applied.

Accepted for publication 12 April 2005Available online 22 June 2005

Int. J. Oral Maxillofac. Surg. 2005; 34: 877–884doi:10.1016/j.ijom.2005.04.017, available online at http://www.sciencedirect.com

0901-5027/080877+08 $30.00/0 # 2005 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

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878 Meijndert et al.

Reliable rehabilitation of the alveolar ridge axis of the implant12,22,34,35. This does not applied: chin bone (N = 5), chin bone in1

Table 1. Personal data and local status of all 15 patients treated for ridge enlargement

Patient Sex Age Site Increase in width atthe top of ridge (mm)

Augmentationmaterial

GBRmembrane

1 F 37 11 4 Chin bone No2 F 44 11 4 Chin bone No3 M 24 21 3 Chin bone No4 M 27 21 2 Chin bone No5 F 38 12 2 Chin bone No

6 M 38 11 4 Chin bone Yes7 F 37 21 3 Chin bone Yes8 M 38 21 2 Chin bone Yes9 F 19 11 3 Chin bone Yes

10 F 37 21 5 Chin bone Yes

11 M 51 14 3 Bio-Oss Yes12 F 29 11 2 Bio-Oss Yes13 F 27 11 3 Bio-Oss Yes14 M 50 12 2 Bio-Oss Yes15 M 26 11 2 Bio-Oss Yes

with endosseous implants requires properquality and quantity of alveolar bone at theimplant site in order to achieve a good long-term prognosis3,11,33. There is a diversity ofsurgical techniques and augmentationmaterials available for improving ridgeconditions that meet these require-ments4,13,14,16,17,24,25,30,32. Such techniquesinclude the use of grafting materials, eitheralone or in combination with barrier mem-branes5,6,15. The most widely applied graft-ing material is autogenous bone, which hasproven its value as grafting material forreconstruction of bony defects13,25,30.Autogenous bone is harvested from bothintra-oral and extra-oral sites. Autogenousbone is considered the ‘‘gold standard’’,but harvesting of autogenous bone requiressurgery at a donor site. This among othersresults in increased morbidity, operationtime and costs18,25,31. These considerationshave led to a search for bone substitutes thatare biocompatible, non-infectious, non-antigenic and resorbable.Reports on ridge augmentation are

merely clinical studies on implant survi-val as a function of the augmentationmaterial used and as a function oftime8,36,37. These clinical data are notindicative for the quality of the bone atthe implantation site in case of recon-struction of local defects3. Histologicalanalysis of the tissue at the implant site isneeded focusing on a detailed character-isation of bone healing and remodelling.Several studies are available focusing ondescriptive histology and histomorpho-metric analysis of autologous bone andbone substitutes. Resorption of autolo-gous bone grafts (up to 56% of corticalbone grafts in 4 months) is reported inboth animal and human studies3,23,27,37.Conflicting results have been reportedregarding the long-term behaviour ofBio-Oss1; some authors have describedsigns of resorption while others havereported a lack of break-down1,2,14,19,23,28,34,35,38. Histomorpho-metric analysis of biopsies taken 4–6months after augmentation show a totalbone volume (TBV) in autologous boneaugmented sites of 37–47%1,3,12. InBio-Oss1 augmented sites a TBV of14–42% newly formed bone is repor-ted after 6 months and a proportionof residual Bio-Oss1 material of 13–30%1,3,12,38.A major drawback of most of the

reports available in literature to date isthat the biopsies taken for analysis arenot derived from the actual implant site.The biopsies are harvested next to theimplant site or perpendicular to the long

provide exact information on the quality ofbone at the actual implant site. The biopsycan show the presence of autogenous boneor a substitute at the biopsy spot while theopposite might be true for the implantationspot. Therefore, the aim of this studywas toinvestigate the quality of the bone at theimplant site by assessing histological andhistomorphometric characteristics of biop-sies taken from the actual implant site andover the full length of the implant section inthe anterior maxilla just prior to implanta-tion. Additionally, clinical assessmentswere performed to compare the histologi-cal and histomorphometric findings withthe clinical characteristics of the peri-implant gingiva.

Materials and methods

Fifteen patients, seven men and eightwomen with a mean age of 32.9 years(range 18–50 years), received an augmen-tation procedure for reconstruction oflocal defect of the anterior maxilla toprovide a basis for reliable insertion ofendosseous dental implants. All patientswere non-smoking, partially edentulousand presented with a single tooth gap(Table 1). In all cases, the implantationsite had to be reconstructed because ofinsufficient bone volume in a buccopalat-inal direction.The defects were located in the ‘‘aes-

thetic zone’’ of the anterior maxilla. Thepre-surgical evaluation disclosed an anat-omy of the local bone responding to a classIV and V according to CAWOOD &HOWELL

7, which did not allow the place-ment of an endosseous implant with suffi-cient initial stability. To reconstruct thesedefects, three treatment modalities were

combination with a Bio-Gide GBR-membrane (Geistlich, Wolhusen, Switzer-land; N = 5) and Bio-Oss1 spongiosagranules (0.25–1.0 mm, Geistlich, Wolhu-sen, Switzerland) in combin ation witha Bio-Gide1 GBR membrane (N = 5)(Fig. 1). A computer software programrandomly placed the participating patientsinto these groups. Informed consent wasobtained from all patients.

Surgical procedures

All patients were treated under localanaesthesia. Antibiotic prophylaxis wasgiven for 72 h (amoxycillin 500 mg + cla-vulanic acid 125 mg (Augmentin1,SmithKline Beecham, Zeist, The Nether-lands), 1 h preoperatively and every 8 hpostoperatively).First a buccal pedunculated and to the

buccal side reflected mucoperiosteal full-thickness flap was raised. From the top ofthe crest the incisions diverged to thebuccolabial fold and were placed in sucha way that the mucoperiosteal flap is oneach side 5 mm wider then the area to beaugmented. The interdental papillae wereincluded in the flap. The extension of theincision to palatal is �5 mm from the topof the crest.After mucoperiosteal reflection the oro-

facial bone width at the implant site wasmeasured to the nearest quarter of a milli-metre using a calliper. The width rangedfrom 1 to 3 mm. The cortical bone on thereceptor site was perforated with a smallround bur in order to create a bleedingbone surface and to open the cancellousbone.Monocortical chin bone grafts (N = 10

patients) were harvested using a bur andchisels and fixed on the perforated recep-

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Bone quality at a reconstructed implant site 879

Fig. 1. Design of the study.

tor site (cortical side to the buccal) with a1.5 mm titanium screw (Martin, Tutlin-gen, Germany)30. Particulated chin bonewas placed around the fixed block graft. Infive patients, the chin bone graft wascovered by a Bio-Gide1 GBR membrane.The membrane was styled with a 3 mmextension over the bone margins of thedefect and fixed with sutures (Vicryl 4-0,Ethicon, Johnson & Johnson, Amersfoort,The Netherlands).Bio-Oss1 granules (N = 5 patients)

were mixed with blood derived from theoperation site and placed on the perforated

cortical bone of the receptor site. A Bio-Gide1 GBR membrane was applied tocover the grafts. The membrane was styledwith a 3 mm extension over the bonemargins of the defect and fixed withsutures (Vicryl 4-0).Three months after augmentation of the

anterior defect in the maxilla with chinbone or 6 months after augmentation withBio-Oss1, the implants were placed.Again, the orofacial bone width at theimplant site was measured to the nearestquarter of a millimetre. The screws used tofix the bonegrafts were removed. Subse-

quently a biopsy was taken from theimplant site using a trephine bur (Ø2.0 mm). Finally, after widening thebiopsy spot to the required dimensionusing standard burs, ITI-EstheticPlus dentalimplants (Institut Straumann AG,Walden-burg, Switzerland) were placed. Theimplants were uncovered 6 months afterplacement.A single operator (GMR) performed all

surgical procedures.At the day of uncovering the implants a

temporary crown was placed, followed bythe placement of the final crown 1 monthlater.

Clinical assessments

Clinical assessments were objectively per-formed at 1 (T0) and 12 months (T12) afterplacement of the final crown using theGingiva Index (GI), pocket probing depth(PPD), and measuring the width of theattached mucosa (WAM) according toestablished methods in the literature (seebelow). Additionally, the level of themarginal buccal gingiva (MBGL)wasmea-sured. All clinical assessments were per-formed by a single investigator (L.M.)(Fig. 1).

1. L

OE & SILNESS Gingiva Index20,21

0 = normal gingiva/mucosa around thetooth;1 = mild inflammation; slight changein colour, slight oedema;2 = moderate inflammation; redness,oedema and glazing;3 = severe inflammation; marked red-

ness and oedema, ulceration.

2. P

ocket probing depth29

Using a Merrit-B perioprobe thedepth of the pocket on the buccal sideof the implant-supported crown wasmeasured. The distance between themarginal border of the gingiva andthe tip of the pocket probe was scoredas the PPD.

3. W

idth of attached mucosa9

The width of the attached mucosabuccal of the implant-supported crownwas measured using the ‘‘Attachedmucosa index’’0 = no keratinised epithelium is avail-able;1 = 1 mm or less keratinised epithe-lium;2 = 1 or 2 mm keratinised epithelium;3 = more than 2 mm keratinised epithe-

lium.

4. L

evel of the buccal marginal gingiva

The level of the buccal marginalgingiva was scored by measuring the

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880 Meijndert et al.

Fig. 2. The level of the buccal marginal gingiva was scored in the midline of the crown bymeasuring the distance between the marginal border of the buccal gingiva and the incisal edge ofthe implant supported crown.

distance between the marginal borderof the buccal gingiva and the incisaledge of the implant supported crown(Fig. 2).

Histology

Biopsies were taken using a 2.0 mm tre-phine bur resulting in specimen with acore diameter of 1.7 mm. The biopsieswere taken at the same location as the‘‘implant-to-be-placed’’, at a similarangulation as the implant and up to a depthof 12 mm. By choosing a trephine bur witha diameter of 2.0 mm, the procedure oftaking the biopsy did not interfere with thepositioning of the implant (diameter4.1 mm). Bio-Oss1 specimens were easierto remove from the trephine than chinbone biopsies. All specimens could beremoved in toto for evaluation.The specimens were fixed in buffered

formalin solution (4%). For histologicprocessing the specimens were washedin 0.185 M sodium cacodylate bufferfor 2 h, dehydrated in ethanol andembedded in light-cured composite mate-rial (Technovit 7200 VLC, Kulzer, Frier-ichsdorf, Germany). Undemineralisedlongitudinal sections were cut from thecentral parts of the biopsies and ground toa thickness of 30 mm according to themethod of DONATH & BREUNER

10. Subse-quently, the sections were surface stainedwith Toluidine blue/Pyronine G and eval-uated histologically and histometrically.

Histological assessments

The biopsies were evaluated with regard tothe vitality of the bone (presence of osteo-cytes in the osteocyte lacunae), signs of

remodelling (presence of osteoblast,osteoıd and osteoclasts) and maturity ofthe bone (woven bone versus lamellarbone). Quantitative evaluation was per-formed with the aid of a light microscopeand the use of ImageAccess (Imagic,Glattbrugg, Switzerland) software. As aregion of interest (ROI) it was decided toanalyse the superior two-thirds of the spe-cimen in order to ensure to predominantlyanalyse grafted material.For the bone histomorphometric ana-

lysis the following values were mea-sured:

1. T

he total bone volume (TBV): the per-centage of the section consisting ofbone tissue.

2. T

he marrow connective tissue volume(MCTV): the percentage of the sectionconsisting of marrow and connectivetissue.

3. T

he remaining Bio-Oss1 volume(RBOV): the percentage of the sectionconsisting of Bio-Oss1 material.

4. T

he total mineralised mass (TMM): thepercentage of the section consisting ofmineralised material (augmentationmaterial (chin bone/Bio-Oss1)/newlyformed bone)

All histological assessments were per-formed by a single investigator (PS) notbeing involved in patient treatment.

Results

None of the 15 patients complained ofsignificant pain either at the donor siteor at the reconstructed local defect sitein the maxilla. Similarly, no objectivesigns of infection were observed. There

was sufficient bone to place implants witha length of 12 mm in all cases. The widthof the orofacial bone at the implant sitegained 2–5 mm (Table 1). Clinically,when compared to the implant sites recon-structed with chin bone grafts, the bone atthe implant site reconstructed with Bio-Oss1 was not as compact as the bone atthe sites reconstructed with chin bone.Nevertheless, the initial stability of theimplants was good in all cases. Noimplants were lost during the follow up.

Clinical assessments

At T0, five implants showed mild inflam-mation (Gingiva Index Score 1), while theother 10 implants had normal peri-implanttissue (Score 0). Twelve months afterplacement of the final crown (T12), oneimplant showed mild inflammation and 14implants had a normal peri-implant gin-giva/mucosa. The mean PPD on the buccalside of the implant-supported crown was3.0 � 1.4 mm at T0 and 3.3 � 1.8 mm atT12. All cases showed an attached mucosaof 2 mm or more around the implant sup-ported crowns. The distance between themarginal border of the buccal gingiva andthe incisal edge of the implant supportedcrown decreased with 0.24 � 1.04 mmbetween T0 and T12.

Histological assessments

Mineralised material with a trabecularbone pattern was found in all biopsiesderived from the augmented areas withsome trabecular bone present in thebiopsies derived from areas grafted withBio-Oss1, and both trabecular and com-pact bone from areas grafted with chinbone. In all groups, a mixture of matureand immature bone was present.In specimen taken from areas grafted

with chin bone, 3 months after grafting,the grafted particles were (partly) sur-rounded by layers of newly formed bone(Fig. 3A). All 10 biopsies from areasgrafted with chin bone contained suchareas. Part of these particles showedempty lacunae suggesting that theseparticles were non-vital, while otherparticles or parts of them clearlyshowed lacunae occupied by osteocytes(Fig. 3B). All chin bone biopsies showedsigns of remodelling as shown by thepresence of osteoblasts, apposition ofosteoıd and resorption lacunae occupiedwith multinuclear osteoclasts. Apposi-tion of bone and remodelling phenomenawere observed on both non-vital andvital chin bone particles. No differences

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Bone quality at a reconstructed implant site 881

Fig. 3. (A) Section of a biopsy specimen after augmentation with chin bone. The biopsy iscomposed of larger and smaller cortical bone particles. Newly formed bone is clearly visible. (B)Detail showing vital, newly formed bone. In most lacunae osteocytes are present.

were observed between biopsies derivedfrom grafted areas that were covered by aresorbable membrane or not. Remnantsof the Bio-Gide1 membrane were notdetected.In specimens taken from the Bio-Oss1

augmented sites, 6 months after grafting,some newly formed bone was present inthe connective tissue surrounding the Bio-Oss1 particles, but most of the particleswere surrounded by connective tissue(Fig. 4A and B). Bio-Oss1 particles werepresent in four out of five biopsies. In thebiopsies with Bio-Oss1 particles neithersigns of inflammation nor signs of foreignbody reaction were seen around the Bio-Oss1 particles. A minority of the particleswas in contact with newly formed vitalbone with lacunae occupied by osteocytes.Thus, at least locally, there seems to besome bone-apposition on the surface of theBio-Oss1 particles (Fig. 4C), but this isnot a general phenomenon 6 months aftergrafting. Although some scalloping ofthe surface of the Bio-Oss1 particleswas noted, no osteoclasts were found inthe specimen. Thus, convincing evidenceof resorption of the Bio-Oss1 particlesor signs of remodelling could not bedemonstrated in our samples. Again, rem-nants of the Bio-Gide1 membrane werenot detected.

Histomorphometry

The mean TBV was in the Bio-Oss1

group significantly lower when comparedto areas grafted with chin bone (p < 0.01,t-test), but the mean TMM was compar-able between the three groups. TheMCTVin the Bio-Oss1 group was comparable tothe MCTV of the chin bone groups. TheRBOV mounted for the remaining part(Table 2).

Discussion

The search for the ideal augmentationmaterial still goes on. Although autologousbone is generally well accepted by most ofthe patients, autologous bone alwaysinvolves donor site surgery and thus donorsite morbidity18,31. Also when mixing allo-graft material with autologous bone, asoften advocated, there still might be a needof an extra donor site in case not sufficientbone can be harvested near the implantsite38. The results of this study indicatethat also buccal grafting of a local defect inthe aesthetic zone of the maxillary alveolarridge with Bio-Oss1 might provide a basisfor reliable placement of implants.The ideal biopsy for histological eva-

luation of the bone at the implant site

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882 Meijndert et al.

Fig. 4. (A) Section of a biopsy specimen after augmentation with Bio-Oss1. The Bio-Oss1

particles are surrounded by connective tissue. Locally vital, newly formed bone is observed. (B)Detail showing the relation between Bio-Oss1 particles, connective tissue and newly formedbone. (C) Detail showing newly formed bone in close contact with a Bio-Oss1 particlesuggesting apposition of bone on the surface of Bio-Oss1 particles. The lacunae in the newlyformed bone contain osteocytes.

should be taken from the actual implantsite and has a diameter and length equal tothe implant. It is possible, as shown in thisstudy, to equal the actual implant lengthand the implant site, but by equalling thediameter of the implant-to-be-placed inthe biopsy there is an inherent risk ofadversely affecting the initial stability ofthe implant. For this reason we used atrephine with a diameter slightly less thanthe diameter of the implant. Even thismethod includes to a certain extent thedeficits of methods harvesting biopsiesnext to the implant site or perpendicularto the long axis of the implant22,34,35 as inone of our biopsies no grafting materialwas detected.The biopsy in which no grafting mate-

rial (Bio-Oss1) was present most likelywas taken from pre-existing autologousalveolar bone just palatal from the aug-mented area not touching the augmenta-tion tissue. This might give rise to theassumption that in this patient augmenta-tion of the defect was not necessary. It isstill possible, however, that after takingthe biopsy (using a 2.0 mm trephine bur)the augmentation material was exposed tothe drill hole side after using the final drillfor the implant surgery (diameter3.8 mm). Alternatively, the applied histo-logical processing technique (only thecentral part of the biopsy) might beresponsible for the absence of augmenta-tion material in the biopsy. But even if theimplant is not in direct contact with thegrafting material, it is thought that aug-mentation is necessary in such cases.Because of a good long-term prognosis,bone grafting is not only applied for goodinitial implant stability, but also to providethe buccal bone plate a minimum thick-ness of 2 mm and to shape the buccalaspect of the jaw. This to try to preventresorption of a thin buccal bone plate andto support the buccal gingiva for an opti-mal aesthetic result of the peri-implantsoft tissues. Furthermore, this observationstresses the purpose of our study, viz. toinvestigate the quality of the bone as closeto the actual implant site as possible.When drawing conclusions from biopsiestaken, e.g. next to the implant site orperpendicular to the long axis of theimplant22,34,35 there is an inherent riskof drawing these conclusions from a mis-concept because the bone quality at theactual implant site might be different fromthe bone in the surrounding area.In all biopsies with Bio-Oss1 granules

present, these granules maintained theirvolume as well showed some osteocon-ductive properties. The granules wereembedded in areas with vital bone, but,

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Bone quality at a reconstructed implant site 883

Table 2. Total bone volume (TBV), marrow connective tissue volume (MCTV), the remaining Bio-Oss1 volume (RBOV) and the totalmineralised mass (TMM)

Mean TBV (%) Mean MCTV (%) Mean RBOV (%) Mean TMM (%)

Chin bone without GBR membrane 55.2 � 6.8 44.8 � 6.8 – 55.2 � 6.8Chin bone with GBR membrane 57.7 � 11.5 42.3 � 11.5 – 57.7 � 11.5Bio-Oss1 with GBR membrane 17.6 � 14.5 41.9 � 13.1 40.5 � 9.3 58.1 � 13.8

as no convincing signs of resorption wereobserved, 6 months after grafting the Bio-Oss1 material was still in place. On thesurface of the Bio-Oss1 particles somescalloping was observed, but presence ofosteoclasts could not been shown. There-fore, it is not possible to state whether thisscalloping is due to post-grafting osteo-clastic activity. Also YILDIRIM et al.38

found no osteoclastic activity after 6months in humans. Other authors suggesta slow but predictable resorption of Bio-Oss1 in humans1,12,34,35. This probablywill occur, but only on the long term asPIATELLI et al.28 observed the presence ofosteoclasts in the process of resorbing theBio-Oss1 particles and formation ofneighbouring newly formed bone in biop-sies retrieved after 18 months and 4 years.These human data are in contrast to animaldata reporting that Bio-Oss1 appears to beprogressively resorbed during a 3–7-month period and became integrated andsubsequently replaced by newly formedbone2,14,19,23.In all areas grafted with chin bone non-

vital bone was still present 3 months afteraugmentation. This is in full agreementwith the study of ZERBO et al.40 reportingthat non-vital bone is replaced by newvital bone in approximately 7 months.Notwithstanding the fact that the heal-

ing time in the Bio-Oss1 group was dou-ble of that of the chin bone groups, 6months after augmentation the majorityof the Bio-Oss1 granules was not replacedby bone. The RBOV found in this study iscomparable to the RBOV reported in theliterature12,26,28,38,39. Obviously, the Bio-Oss1 group can be expected to rendersmaller values for the TBV than chin bonegroups due to the fact that part of thedefect space is filled with Bio-Oss1 par-ticles. When the RBOV is added to thecalculation, similar values for the TMMwere obtained for the Bio-Oss1 group andthe chin bone groups. Despite the rela-tively low osteoinductive capacity of sym-physial bone compared to otherautologous bone grafts, it is still superiorto Bio-Oss1 considering the difference inhealing time (3 months) needed to achievethe same results.It was noted that the initial stability of

the implants was good in all casesalthough the bone at the implant sites

reconstructed with Bio-Oss1 clinicallywas not as compact as the bone at sitesreconstructed with chin bone. A possibleexplanation for this is that in the Bio-Oss1

cases the apical part of the implants couldhave been inserted in pre-existing alveolarbone, in which case the support of the pre-existing alveolar bone is responsible forthe good initial stability of the implantsrather than the Bio-Oss1 augmentationmaterial. As it takes more than 6 monthsfor the implants to be loaded (abutmentconnection is performed 6 months afterimplant placement) further ingrowth ofbone and suggested remodelling of thegrafting material probably will haveoccurred thus allowing for loading ofthe implants.From this study, it is concluded that at

the time of placement of the implants thegrafting material is still not fully replacedby new vital bone. In case of Bio-Oss1,most of the grafting material is even stillpresent. Despite these differences, the 1-year clinical results were very good andcomparable between the various graftingtechniques applied.

Acknowledgment. We are very grateful forthe financial support of this study byGeistlich, Wolhusen, Switzerland.

References

1. Araujo MG, Sonohara M, Hayaci-

bara R, Cardaropoli G, Lindhe J.Lateral ridge augmentation by the useof grafts comprised of autologous boneor biomaterial. An experiment in the dog.J Clin Periodontol 2002: 29: 1122–1131.

2. Berglundh T, Lindhe J. Healingaround implants placed in bone defectstreated with Bio-Oss1. An experimentalstudy in the dog. Clin Oral Implant Res1997: 8: 117–124.

3. Blomqvist JE, Alberius P, Isaksson S,Linde A, Obrant K. Importance of bonegraft quality for implant integration aftermaxillary sinus reconstruction. Oral SurgOral Med Oral Pathol Oral Radiol Endo-dond 1998: 86: 268–274.

4. Breine U, Branemark P-I. Reconstruc-tion of alveolar jaw bone. Scand J PlasticReconstr Surg 1980: 14: 14–48.

5. Buser D, Bragger U, Lang NP, Nyman

S. Regeneration and enlargement of jawbone using guided tissue regeneration.Clin Oral Implant Res 1990: 1: 22–32.

6. Buser D, Schenk RK, Belser U, Hirt

HP, Berthold H. Localized ridge aug-mentation using guided bone regenera-tion. 1. Surgical procedure in themaxilla. Int J Periodont Restorative Dent1993: 13: 29–45.

7. Cawood JJ, Howell RA... Classificationof the edentulous jaws. Int J Oral Max-illofac Surg 1988: 17: 232–236.

8. Cordaro L, Sarzi Amade D, Cordaro

M. Clinical results of alveolar ridge aug-mentation with mandibular block bonegrafts in partially edentulous patientsprior to implant placement. Clin OralImplant Res 2001: 13: 103–111.

9. Cox JF, Zarb GA. The longitudinal clin-ical efficacy of osseointegrated dentalimplants: a 3-year report. Int J Oral Max-illofac Implants 1987: 2: 91–100.

10. Donath K, Breuner G. A method forthe study of undecalcified bones and teethwith attached soft tissues. The Sage–Schliff (sawing and grinding) technique.J Oral Pathol 1982: 11: 318–326.

11. Esposito M, Hirsch J-M, Lekholm U,Thomsen P. Biological factors contribut-ing to failures in osseointegrated oralimplants. (II) Etiopathogenesis. Eur JOral Sci 1998: 106: 721–764.

12. Friedmann A, Strietzel FP,Maretzki

B, Pitaru S, Bernimoulin JP. Histolo-gical assessment of augmented jaw boneutilizing a new collagen barrier mem-brane compared to a standard barriermembrane to protect a granular bonesubstitute material. A randomized clinicaltrial. Clin Oral Implant Res 2003: 13:587–594.

13. Garg AK, Morales MJ, Navarro I,Duarte F. Autogenous mandibular bonegrafts in the treatment of the resorbedmaxillary anterior alveolar ridge: ratio-nale and approach. Implant Dent 1998: 7:169–176.

14. Hammerle CHF, Chiantella GC, Kar-

ring T, Lang NP. The effect of a depro-teinized bovine bone mineral on boneregeneration around titanium dentalimplants. Clin Oral Implant Res 1998:9: 151–162.

15. Hurzeler MB, Kohal RJ, Mota L,Naghshbandi J, Caffesse RG. A newbioresorbable barrier to facilitate guidedbone regeneration. J Dent Res 1997: 76:167.

16. Hurzeler MB, Quinones CT, Kirsch

A, Gloker C, Schupbach P, Strub JR,Caffesse RG. Maxillary sinus augmenta-tion using different grafting materials anddental implants in monkeys. Part I. Eva-luation of anorganic bovine-derived bone

Page 9: University of Groningen Bone quality at the implant site ... · isation of bone healing and remodelling. Several studies are available focusing on descriptive histology and histomorpho-metric

884 Meijndert et al.

matrix. Clin Oral Implant Res 1997: 8:476–486.

17. Jensen SS, Aaboe M, Pinholt EM,Hjørting-Hansen E, Melsen F, Ruy-

ter IE. Tissue reaction and material char-acteristics of four bone substitutes. Int JOral Maxillofac Implants 1992: 7: 233–245.

18. Kalk WWI, Raghoebar GM, Jansma J,Boering G. Morbidity from iliac crestbone harvesting. Clin Oral Implant Res1996: 54: 1424–1429.

19. Klinge B, Alberius P, Isaksson S,Jonsson J. Osseous response toimplanted natural bone mineral andsynthetic hydroxylapatite ceramic inthe repair of experimental skull bonedefects. Clin Oral Implant Res 1992:50: 241–249.

20. Loe H. The gingival index, the plaqueindex and the retention index systems. JPeriodontol 1967: 38: 610–616.

21. Loe H, Silness J. Periodontal disease inpregnancy. II: Correlation between oralhygiene and periodontal condition. ActaOdontol Scand 1963: 21: 533–551.

22. Matsumoto MA, Filho HN, Fran-

cischone CE, Consolaro A. Micro-scopic analysis of reconstructedmaxillary alveolar ridges using autoge-nous bone grafts from the chin and iliaccrest. Int J Oral Maxillofac Implants2002: 17: 507–516.

23. Merkx MAW, Maltha JC, Freihofer

HP, Kuijpers-Jagtman AM. Incorpora-tion of particulated bone implants in thefacial skeleton. Biomaterials 1999: 20:2029–2035.

24. Misch CE, Dietsh F. Bone graftingmaterials in implant dentistry. ImplantDent 1993: 2: 158–167.

25. Misch CM. Comparison of intraoraldonor sites for onlay grafting prior toimplant placement. Int J Oral MaxillofacImplants 1997: 12: 767–776.

26. Norton MR, Odell EW, Thompson ID,Cook RJ. Efficacy of bovine bonemineral for alveolar augmentation: ahuman histologic study. Clin OralImplant Res 2003: 14: 775–783.

27. Ozaki W, Buchman SR. Volume main-tenance of onlay bone grafts in the cra-niofacial skeleton: micro-architectureversus embryologic origin. Plast ReconstrSurg 1998: 102: 291–299.

28. Piattelli M, Favero GA, Scarano A,Orsini G, Piattelli A. Bone reactions toanorganic bovine bone (Bio-Oss) used insinus augmentation procedures: a histo-logic long-term report of 20 cases inhumans. Int J Oral Maxillofac Implants1999: 14: 835–840.

29. Quirijnen M, Naert I, Van Steen-

berghe D, Teerlinck J, Dekeyser C,Theuniers G. Periodontal aspects ofosseointegrated fixtures supporting anoverdenture. A 4-year retrospectivestudy. J Clin Periodontol 1991: 18:719–728.

30. Raghoebar GM, Batenburg RHK,Vissink A, Reintsema H. Augmentationof localized defects of the anterior max-illary ridge with autogenous bone beforeinsertion of implants. J Oral MaxillofacSurg 1996: 54: 1180–1185.

31. Raghoebar GM, Louwerse C, Kalk

WWI, Vissink A. Morbidity of chin boneharvesting. Clin Oral Implant Res 2001:12: 503–507.

32. Tadjoedin ES, de Lange GL, Lyaruu

DM, Kuiper L, Burger EH. High con-centrations of bioactive glass material(BioGran) vs. autogenous bone for sinusfloor elevation. Clin Oral Implant Res2002: 13: 428–436.

33. Truhlar RS, Orenstein IH, Morris

HF, Ochi S. Distribution of bone qualityin patients receiving endosseous dentalimplants. J Oral Maxillofac Surg 1997:55: 38–45.

34. Valentini P, Abensur D, Densari D,Graziani JN, Hammerle CHF. Histolo-gical evaluations of Bio-Oss1 in a2-stage sinus floor elevation and implan-tation procedure. A human case report.Clin Oral Implant Res 1998: 9: 59–64.

35. Valentini P, Abensur D, Wenz B,Peetz M, Schenk R. Sinus grafting withporous bone mineral (Bio-Oss1) forimplant placement: a 5 year study on

15 patients. Int J Periodont RestorativeDent 2000: 20: 245–253.

36. Von Arx T, Cochran DL, Hermann JS,Schenk RK, Higginbottom FL, Buser

D. Lateral ridge augmentation andimplant placement: an experimental studyevaluating implant osseointegration indifferent augmentation materials in thecanine mandible. Int J Oral MaxillofacImplants 2001: 16: 343–354.

37. Widmark G, Andersson B, Ivanoff CJ.Mandibular bone graft in the anteriormaxilla for single-tooth implants. Presen-tation of surgical method. Int J Oral Max-illofac Surg 1997: 26: 106–109.

38. Yildirim M, Spiekermann H, Biester-

feld S, Edelhoff D. Maxillary sinusaugmentation using xenogenic bone sub-stitute material Bio-Oss1 in combinationwith venous blood. A histologic and his-tomorphometric study in humans. ClinOral Implant Res 2000: 11: 217–229.

39. Yildirim M, Spiekermann H, Handt S,Edelhoff D. Maxillary sinus augmenta-tion with the xenograft Bio-Oss1 andautogenous intraoral bone for qualitativeimprovement of the implant site: a histo-logic and histomorphometric clinicalstudy in humans. Int J Oral MaxillofacImplants 2001: 16: 23–33.

40. Zerbo IR, De Lange GL, Joldersma M,Bronckers ALJ, Burger EH. Fate ofmonocortical bone blocks grafted in thehuman maxilla: a histological and histo-morphometric study. Clin Oral ImplantRes 2003: 14: 759–766.

Address:Leo MeijndertDepartment of Oral andMaxillofacial Surgery and MaxillofacialProsthetics

University Medical Center Groningenand University of Groningen

P.O. Box 30.0019700 RB GroningenThe NetherlandsTel: +31 50 3613840Fax: +31 50 3611136E-mail: [email protected]