Histological Comparison of Healing Extraction Sockets Implanted With Bioactive Glass or...

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Histological Comparison of Healing Extraction Sockets Implanted With Bioactive Glass or Demineralized Freeze Dried Bone Allograft: A Pilot Study Stuart Froum.* Sang-Choon Cho,* Edwin Rosenberg,* Michael Rohrer/ and Dennis Tarnow* Background: Various materials have been used immediately fol- lowing tooth extraction to fill and/or cover the socket in an attempt to limit or prevent ridge resorption. The purpose of the present pilot study was to establish a reliable model to investigate the effect of var- ious bone graft and bone replacement materials on extraction socket healing. This study also compared healing extraction sockets 6 to 8 months postimplantation of a bioactive glass (BG) or demineralized freeze-dried bone allograft (DFDBA) to an unfilled socket control (C). Methods: Following tooth extraction, a total of 30 sockets in 19 patients were randomly divided into 3 treatment groups: 10 sockets received BG, 10 sockets DFDBA, and 10 sockets served as unfilled controls. Primary coverage was achieved by flap advancement over each socket. Six to 8 months postextraction at time of implant place- ment, histological cores of the treatment sites were obtained. These cores were processed, undecalcified sections prepared and stained with Stevenel blue/van Gieson's picric fuchsin, and histomorphome- trically analyzed. Vital bone, connective tissue and marrow, and resid- ual graft particles were reported as a percentage of the total core. Results: A model system was described in humans and used to evaluate the healing response in the 3 treatment groups. Results con- cluded that mean vital bone present was 59.5% for BG-, 34.7% for DFDBA-, and 32.4% for C-treated sites. These differences were not statistically significant. However, the residual implant material was significantly higher in DFDBA-treated (13.5%) versus BG-treated sockets (5.5%). Conclusions: Although the differences in percent vital bone were not statistically significant among the 3 treatment groups in this pilot study, BG material was observed to act as an osteoconductive mate- rial which had a positive effect on socket healing at 6 to 8 months postextraction. Further research following implant placement in treated and control sockets is warranted to determine if bone implant con- tact is improved in BG-filled versus unfilled sockets. J Periodorttol 2002:73:94-102. KEY WORDS Alveolar bone loss/prevention and control; tooth extraction; wound healing; grafts, bone; glass, biologically active; follow-up studies. * Ashman Department of Implant Dentistry. Mew York University. Kriser Dental Center. Mew York. MY. t Division of Oral and Maxillofacia] Pathology, University of Minnesota, School of Dentistry. Minneapolis, MN. t Ashman Department of Implant Dentistry and Department of Persodontology. Mew York University. R oot form implants have demonstrated a high degree of successful osseointegration in both fully and partially edentu- lous patients. 1 4 However, in order for these implants to be placed in a favorable prosthetic position for sub- sequent restoration, it is often nec- essary to augment existing alveolar bone. Numerous biocompatible mate- rials have been used in an attempt to correct hard tissue ridge defor- mities and thus allow ideal implant placement. These materials include intra- and extraoral autogenous bone; demineralized freeze-dried bone allografts (DFDBA): and var- ious alloplasts, xenografts, bone substitutes, and membrane barri- ers. 5 " 8 Success rates of implants placed in this regenerated bone are comparable to the success rates of implants in natural bone. 9 " 11 How- ever, increased patient morbidity, cost, and time accompany these attempts to regenerate lost soft and hard tissues. In most cases a 6- to 12-month healing period is neces- sary following augmentation sur- gery before implants can be placed. Some of the main causes of alveolar bone deformities which require augmentation procedures are the bone resorption and heal- ing patterns that take place follow-

Transcript of Histological Comparison of Healing Extraction Sockets Implanted With Bioactive Glass or...

Histological Comparison of HealingExtraction Sockets Implanted WithBioactive Glass or Demineralized FreezeDried Bone Allograft: A Pilot StudyStuart Froum.* Sang-Choon Cho,* Edwin Rosenberg,* Michael Rohrer/ and Dennis Tarnow*

Background: Various materials have been used immediately fol-lowing tooth extraction to fill and/or cover the socket in an attemptto limit or prevent ridge resorption. The purpose of the present pilotstudy was to establish a reliable model to investigate the effect of var-ious bone graft and bone replacement materials on extraction sockethealing. This study also compared healing extraction sockets 6 to 8months postimplantation of a bioactive glass (BG) or demineralizedfreeze-dried bone allograft (DFDBA) to an unfilled socket control (C).

Methods: Following tooth extraction, a total of 30 sockets in 19patients were randomly divided into 3 treatment groups: 10 socketsreceived BG, 10 sockets DFDBA, and 10 sockets served as unfilledcontrols. Primary coverage was achieved by flap advancement overeach socket. Six to 8 months postextraction at time of implant place-ment, histological cores of the treatment sites were obtained. Thesecores were processed, undecalcified sections prepared and stainedwith Stevenel blue/van Gieson's picric fuchsin, and histomorphome-trically analyzed. Vital bone, connective tissue and marrow, and resid-ual graft particles were reported as a percentage of the total core.

Results: A model system was described in humans and used toevaluate the healing response in the 3 treatment groups. Results con-cluded that mean vital bone present was 59.5% for BG-, 34.7% forDFDBA-, and 32.4% for C-treated sites. These differences were notstatistically significant. However, the residual implant material wassignificantly higher in DFDBA-treated (13.5%) versus BG-treatedsockets (5.5%).

Conclusions: Although the differences in percent vital bone werenot statistically significant among the 3 treatment groups in this pilotstudy, BG material was observed to act as an osteoconductive mate-rial which had a positive effect on socket healing at 6 to 8 monthspostextraction. Further research following implant placement in treatedand control sockets is warranted to determine if bone implant con-tact is improved in BG-filled versus unfilled sockets. J Periodorttol2002:73:94-102.

KEY WORDSAlveolar bone loss/prevention and control; tooth extraction; woundhealing; grafts, bone; glass, biologically active; follow-up studies.

* Ashman Department of Implant Dentistry. Mew York University. Kriser Dental Center. Mew York. MY.t Division of Oral and Maxillofacia] Pathology, University of Minnesota, School of Dentistry.

Minneapolis, MN.t Ashman Department of Implant Dentistry and Department of Persodontology. Mew York University.

Root form implants havedemonstrated a high degreeof successful osseointegration

in both fully and partially edentu-lous patients.1 4 However, in orderfor these implants to be placed in afavorable prosthetic position for sub-sequent restoration, it is often nec-essary to augment existing alveolarbone.

Numerous biocompatible mate-rials have been used in an attemptto correct hard tissue ridge defor-mities and thus allow ideal implantplacement. These materials includeintra- and extraoral autogenousbone; demineralized freeze-driedbone allografts (DFDBA): and var-ious alloplasts, xenografts, bonesubstitutes, and membrane barri-ers.5"8 Success rates of implantsplaced in this regenerated bone arecomparable to the success rates ofimplants in natural bone.9"11 How-ever, increased patient morbidity,cost, and time accompany theseattempts to regenerate lost soft andhard tissues. In most cases a 6- to12-month healing period is neces-sary following augmentation sur-gery before implants can be placed.

Some of the main causes ofalveolar bone deformities whichrequire augmentation proceduresare the bone resorption and heal-ing patterns that take place follow-

J Periodoncol • January 2002 Froum, Cho, Rosenberg, Rohrer, Tarnow

ing tooth extraction.121 :l Controlled clinical studieshave documented an average of 4.0 to 4.5 mm ofhorizontal bone resorption following routine atraumatictooth extraction.1415 Other studies have documentedsignificant dimensional changes in the surroundingalveolar bone following extraction procedures.16"18

One study documented that 31 of 34 (91%) patientswho were partially edentulous in the maxillary ante-rior area had some ridge defect.19

In an attempt to preserve alveolar bone and avoidthe necessity of ridge augmentation prior to implantplacement, various materials have been used imme-diately following tooth extraction to fill and/or cover thesocket. While many of these studies showed positiveclinical results, histological evaluation of grafted sock-ets has shown mixed results.

Two separate histological studies reported positivesocket healing responses with alloplasts20 and axenograft21 while others have shown poor results withDFDBA, bovine bone, and even autogenous bone whenimplanted into sockets following tooth extraction.2221

In fact, one study concluded that the latter 3 graftmaterials interfered with the normal socket healingand therefore should not be used for socket treat-ment.22 However, many variables, including type andsize of defect, type of graft, implant or barrier used,time of healing response, flap closure and lack of con-trols, as well as differences in host response, to namea few, make study comparisons and conclusions dif-ficult. Moreover, these studies were, for the most part,case reports which are of interest but do not providea reliable understanding of factors that affect the qual-ity and quantity of bone and timing for the optimalimplant placement.

It is therefore important to minimize as many vari-ables as possible in order to better evaluate the effectsof materials and techniques utilized to preserve alve-olar bone following tooth extraction in a site diagnosedto receive a root form implant. The purpose of thepresent study was to establish a reliable model to inves-tigate the effect of various bone graft and bone replace-ment materials on the healing of an extraction socket.This pilot study was designed to histologicaliy evalu-ate the healing of extraction sockets 6 to 8 monthsfollowing implantation of a bioactive glass or demin-eralized freeze-dried bone allograft compared to nograft at all.

MATERIALS AND METHODS

Study PopulationThirty (30) teeth scheduled for extraction for peri-odontal or prosthetic reasons were selected in 19patients (12 males; 7 females; age range 35 to 77years) who presented to the Ashman Department ofImplant Dentistry at Hew York University Kriser Den-tal Center. The diagnosis of these teeth for extraction

was confirmed by 2 separate instructors who were notpart of the present study. All patients met the previ-ously established physical and psychological criteriafor implant treatment in the Department of ImplantDentistry. In addition, patients did not have any med-ical conditions and were not taking any medicationsthat were associated with a compromised bone healing response (i.e., diabetes, autoimmune dysfunction,prolonged cortisone therapy, or chemotherapy). Allpatients were non-smokers or previous smokers whohad not smoked for at least 6 months. All patients hadno known allergies to tetracycline and had not receivedany antibiotic over the previous 6 months. Patientswere given an explanation of the nature of the studyand. after expressing a wish to participate, they signeda written consent form prior to their participation. Theinformed consent and instruction to patient forms aswell as the study protocol were approved by the Clniversity Committee on Activities Involving Human Sub-jects.

Participating patients were told that if they decidedto discontinue their participation in the study at anytime they could continue being treated at New YorkUniversity Dental Center as a regular clinic patient.

MeasurementsPrior to extraction radiographs, impressions, and diag-nostic casts were taken. A template was then fabri-cated on the study model including at least one toothanterior or posterior to the hopeless tooth. A light curedresin material'' was used to fabricate the template. Thecrown of the hopeless tooth was cut off on the studymodel and a guide hole was drilled with a 3 x 10 drill"through the template directly above the outline of theroot on the model. A metal ring (Fig. 1) was placedin the hole and resin added around the ring to stabilize its position. At time of implant surgery (6 to 8months following extraction) the template was againpositioned in order to take a histological core from theidentical site.

Surgical ProtocolFollowing administration of local anesthesia, crestaland intrasulcular incisions were made to expose theinvolved roots and alveolar crest. Buccal and lingualflaps were raised to adequately view the sockets andallow sufficient flap release to obtain primary closure.After extraction of the tooth the sockets were debrided,measured, and decorticated with a Vz round bur undercopious irrigation (Fig. 2).

Following tooth extraction, those sockets with <2mm of buccal plate bone loss were included in thestudy. Thus each of the sockets treated had a 4-wallconfiguration. Treatment selection was then made ran-

§ Triad, Dentsply International, York, PA.|| ITI Institute Straumann, Waldenburg. Switzerland.

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Extraction Socket Healing After Implants With Bioactive Glass or DFDB Allograft Volume 73 • Number I

Figure I.• in study model containing ihe

•;g positioned met (tie central area of the extinction socket

Figure 2.The ilebridedand decorticated socket with 4 remaining waHs inducingfire bucca! plate.

Figure 3.Buxjrf/ve glass being compressed into the socket.

Figure 4.'in flop is sutured to obtain complete socket coverage.

domly from sealed envelopes prepared by a statisti-cian. Of the 30 sockets treated. 10 sockets receiveda bioactive glass material (BQ), 10 sockets receiveddemineralized freeze-dried bone allograft (DFDBA). and10 sockets (C) served as unfilled controls. Treatmentconsisted of socket debridement alone (C). debride-ment followed by implantation of BG, or debridementfollowed by implantation of DFDBA. The freeze-driedbone allograft was obtained from an accredited com-mercial bone bank^l and consisted of cortical bone of250 to 500 u sized particles. The bioactive glass* hada limited particle size of 300 to 355 jam. Both materi-als were hydrated with sterile saline at least 15 min-utes prior to insertion in the socket and then packedinto the socket (Fig. 3). Flaps were then sutured with4-0 silk utilizing interrupted and vertical mattresssutures. In all cases tension-free primary closure wasachieved and the temporary prosthesis was relieved

prior to insertion (Fig. 4). Patients were placed ondoxycycline 100 mg beginning at least 1 hour prior tosurgery and continuing for 13 days following surgery.Patients were also prescribed 0.12% chlorhexidinerinses** twice a day beginning the day after surgeryand continuing for 30 days following surgery. Sutureswere removed 7 to 14 days following surgery.

Six to 8 months following extraction socket surgery,an implant of appropriate size was placed in the healedsocket. At time of implant site preparation the templatewas again placed and a core of bone 2.0 mm x 7.0mm long (Figs. 5 and 6) was obtained with the samesize trephine used previously. The cores were codedand sent to the Hard Tissue Research Laboratory at theUniversity of Oklahoma College of Dentistry. The pro-

1 University of Miami Bone Bank, Miami School of Medicine. Miami. FL# Biogran. Orthovita. Malvern, PA.** Peridex. Procter & Gamble, Cincinnati, OH.

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Periodontol • January 2002 Froum, Cho, Rosenberg, Rohrer, Tar now

Figure 5.At time 0/ implant placement (6 to 8 months following sockettreatment) the template : iitionedand the trephine placedihiotigh the metal ring to obtain <i cots 0/ bone from the healingsocket

Figure 6.f?ie / ( ' x 7.0 nun core 0} tone from the healing socket

cessing and histomorphometric measurements wereperformed by an investigator who had no knowledgeof the treatment rendered. The cores were stained withStevenel blue/van Gieson's picric fuchsin and histo-morphometrically analyzed for bone and soft tissue.Processing and analysis of the specimens using a non-decalcified technique has been described.?A Values

Figure 7.'''••I (traction radiograph 0/ the hope/ess maxillary right centra) incisor

were then reported using a grid overlay for total bonematerial, percent vital bone, percent connective tissue(% CT). and percent residual implant materials (%RIM).

RESULTSAll sites healed uneventfully (Figs. 7 and 8). Meanvital bone measurements for BG, C, and DFDBAgroups were as follows: 59.5%, 32.4%, and 34.7%,respectively (Figs. 9, 10, and 1 1) (Table I). The rangeof vital bone was 22 to 88% for BG-, 17 to 53.1% forC-, and 23 to 48.1% for DFDBA-treated sites (Table2). Connective tissue percentages averaged 35.3% forBG, 67.0% for C, and 51.6% for DFDBA. The BG-treated sockets showed 5.5% residual implant mater-ial while the DFDBA-treated sockets had 13.5% resid-ual implant material. All bone present in control andbioactive glass-treated sockets was reported as 100%vital. Bone present at the demineralized freeze-driedbone treated sites was 100% vital in 7 sockets and 50%.74%, and 80% vital in 3 remaining sockets. Mew boneand osteoid was observed surrounding the remainingBG particles (Fig. 12). Mew bone was not only seen atthe periphery, but also in the internal pores of the BGparticles (Fig. 13). In sections containing remainingDFDBA particles, non-vital bone was observed in closeproximity to reossifiying areas (Fig. 14). This patternof reossification was observed to varying degrees withthe remaining non-vital DFDBA particles.

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Extraction Socket Healing After Implants With Bioactive Glass or DFDB Allograft Volume 73 • Number

Figure 8.'•-..- , months postsurgico) radiogroph oj a socket filled with bioactive

Figure 10.A low power histotogkxiJ section of b'/i-month posiextracmxi core of aBG-treoted sorfcef. Vittj/ bone measured 50%. (Origino/ mognificotronx/.'>: Stevene/'s Bluelwn Gesm's inaic fuchsin stain.)

Statistical AnalysisThirty (30) sites in 19 different patients were ran-domized to each of 3 treatments. The patients included7 females and 12 males with a mean age of 54.9 years(SD = 1 1.9; range: 35 to 77). At the 6- to 8-month fol-lowup. data were collected for the percentage CT, thepercentage RIM, and the percentage vital bone. Gsingthe method of generalized estimating equations (GEE)

Figure 9.Low power histological section of a core of bone obtained 8 months.postgrafiing with DFDBA. Vnol bone measured 48%. (Originalmagnification x?.5:Stevenel's Blue/van Geson's picric fuchsin itam.)

Figure 11.A Iowa power htstologicol section of an 8-month posiextractjon coreof an ungraftcd (control) . tone measured 34% (Ongmalmagnification x2.5; Stevenel s blue/van Gjeson's picric fuchsin stain.)

with an exchangeable working correlation, the meanpercent CT, mean percent RIM. and mean percent vitalbone were compared among the 3 treatment typesused. Adjusted means with corresponding confidenceintervals were calculated using GEE and are given inTable 1. The mean percent CT varied by treatmenttype. In particular, treatment type B yielded a signifi-cantly lower percent CT compared to either type C ortype D. The mean percent RIM varied by treatmenttype with all treatments differing significantly from eachother. Although the percent vital bone for treatmenttypes C and D appeared to be significantly differentfrom the percent vital bone for treatment type B, theoverall differences failed to achieve statistical signifi-cance (P= 0.074).

J Periodontol * January 2002 Froum, Cho, Rosenberg, Rohrer, Tarnow

Table I.

Adjusted Means by Treatment Type

Parameter Type

Adjusted

Mean (%)

Confidence

Interval

,CT

%RIM

% vital bone

B

C

D

BC[)

BCD

35.397051.6

sio.o

13.5

59.532.434.7

(21.2.49.5)(60.9,73.2)(43.5,59.6)

(4.3, 6.7)(0,0)(9.9, 17.2)

(45.2. 73.7)(26,3. 38.4}(26.8,42.5)

0.006

0.001

0.074

B = BG; C Control; D = DFDBA.

DISCUSSIONThe first goal of the present study was to establish ahuman model system to evaluate the healingresponse of various materials used to promote boneformation. It is recognized that differences in the hosthealing response make identical comparisons inhumans impossible. However, the size and type ofbone defects following tooth extraction often presentsimilar healing environments. To further standardizeour model we chose to include only those socketswith 4 remaining walls. In addition, sockets wererequired to have 2 mm or less of the buccal platemissing following extraction. This measurement wasmade in comparison with the buccal bone on theadjacent tooth or teeth at time of tooth extraction.

Since the socket healing response is mediated bythe surrounding bony walls, this requirement servedto standardize the model system.25 Several measureswere taken to ensure that the histological specimenwould consist of the healing rather than the nativebone. First, the template and metal ring allowed exactpositioning of the trephine over the healing site. Sec-ond, a narrow trephine (2 mm internal diameter) wasused and only a 7 mm core was obtained. The coro-nal reference point for this core was the distancebetween the template and bucca! crest immediatelyfollowing tooth extraction.

All specimens were stained with Stevenel blue/vanGieson's picric fuchsin.?4 This allowed a more accu-rate calculation of vital bone. Moreover, since theinvestigator performing the histomorphometric analy-sis had no knowledge of what procedure was per-formed in the socket, measurement bias was con-trolled. Lastly and most importantly in our humanmodel system was the fact that a root form implantwas placed into the same area from which the corewas obtained. Since the implant was of larger diam-

Table 2.

Data of 30 Sockets Treated With EitherBioactive Glass, Gngrafted Control, orDemineralized Freeze-Dried Bone Allografts

Patient

SI

SI

w

LI

B

LI

S2

M

K

F

SI

PI

LI

Y

L2

K

•1

P2

B

S3

SI

SI

c

G

G

L3

B

HI

H2

L4

B = BG. C

Type

B

B

B

B

B

B

B

B

B

B

C

C

c

c

c

c

cc

cc

D

D

D

D

D

D

D

D

D

D

Gen-

der

M

M

M

F

M

F

M

F

F

I

M

F

1

M

M

F

F

F

F

M

M

M

M

M

M

M

M

F

M

M

= Control, D =

Age

66

66

62

61

60

61

46

50

47

77

66

55

(,l

50

51

47

56

67

75

36

66

66

35

60

70

47

60

65

42

43

DFDBA.

Tooth

25

27

5

23

8

26

18

20

22

8

22

II

24

15

28

27

7

20

4

10

23

21

8

5

12

23

9

18

18

15

Months

8

8

8

6

6

6

6

6

8

6

8

6

6

6.5

(,

8

6

6.5

6

8

8

8

6

6

6

6

6

6

8

6

%C\

25

27

44

72

28

61

43

II

10

66

60

64

78

70

60

66

65

75

83

46.9

60

60

44

54

40

41

42

44.4

43.2

60

% RIM

3

3

3

6

5

4

7

7

2

6

0

0

0

0

0

0

0

0

0

0

8

10

10

16

18

17

8

26

8.7

17

% Vital

Bone

72

70

53

22

67

35

50

82

88

28

40

36

22

30

40

34

35

25

17

53.1

32

30

46

30

42

42

50

29.6

48,1

23

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Extraction Socket Healing After Implants With Bioactive Glass or DFDB Allograft Volume 73 * Number

Figure 12.A b-manth medium power view oj remaining BG particles, surroundedby mature vital tone and osteoid (green). (Original magnification xl 0;Stevenel's blue/van Geson's picric fucbsin stain.)

Figure 14,A medium power histologkal specimen oj DFDBA particles undergoingfeossification, Foti oj the ossifying area is seen with newly formingosteoid (green) in close proximity. (Original magnification x20:Sterene/'s Blue/van Gieson's picric fuchsm stain.)

Figure 13.A higher power hJsfo/ogiraf specimen of the HG partides with aieas ofnew bone forming on the periphery and within tlie pores oj the.particles. (Original magnification xlb; Stsvenel's Blue/van Gieson'spiaic fuchsm stain.)

eter and length that the 2.0 mm by 7.0 mm core, thisavoided any additional insult to the patient.

The second goal of the study was to compare sockethealing of two implanted materials, demineralized freeze-dried bone (DFDBA) and bioactive glass (BG) of lim-ited particle size, with healing of an ungrafted socket(control). Although each of the 3 groups containedonly 10 sockets, healing trends were obvious. The BG-treated sockets showed more vital bone (59.5%) at 6to 8 months postextraction than either the DFDBA-treated sockets (34.7%) or the C sockets (32.4%).Moreover the amount of residual implanted material(RIM) was higher with DFDBA- (1 3.5%) than with BG-treated (5.5%) sockets.

Although the percent vital bone of the BG-treatedsites was greater than either the DFDBA- or control-treated sites, this difference was not statistically sig-nificant. The small sample size in this study contributedto this statistical finding. However, the clinician mayfind this difference in healing response clinically rele-vant. While we did not calculate the differences in vitalbone in the coronal versus apical part of our cores aswas done by Artzi et al,21 the overall average vitalbone in our BG cores at 6 to 8 months postextractioncompared favorably with the cancellous porous bovinebone mineral (PBBM)-treated sockets at 9 months post-extraction (average 46.3%) as they reported. More-over, the residual volume of PBBM (approximately30%) was greater than that of the remaining BG (5.5%)found in the present study. This difference may beattributed to a more rapid absorption of BG particles.

The results seen in the present study, which demon-strate more bone at 6 to 8 months in the BG-treatedsockets than the ungrafted sockets, may be attributedto the osseoconductive nature of the BG particles. Adirect chemical bond by BG to bone has been shownin previous studies.26 Moreover, the absorbable BGmaterial has been shown to be biocompatible and non-toxic.

The bioactive glass particles have been shown tobecome coated by a calcium-phosphate (Ca-P) layerin vivo.26 This Ca-P rich layer is equivalent to the min-eral phase of bone and is responsible for the osteo-conductive properties. The particles themselves areeroded internally by phagocytic cells which absorb sil-ica rich contents of the particles to further expose theCa-P rich layer to interstitial fluids. Mew bone thenforms within and external to the particles. Remodel-

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J Periodontol • January 2002 Froum, Cho, Rosenberg, Rohrer, Tar now

ing of the particles is accompanied by replacementwith bone tissue (Fig. 13).

Furusawa and Mizunuma27 utilized bioactive glass inthe repair of surgically created bony defects in the ratmandible and found osteoconductive bone growtharound the particles by 4 weeks. Cancian et al.28 com-pared bioactive glass, dense hydroxyapatite (HA), andan unfilled control to study the healing of surgically cre-ated cavities in the angle region of the mandible in 4adult monkeys. At 180 days postsurgery, no bone for-mation was observed in the empty cavity, total bonerepair of the bone defect in the bioglass-treated sites, andno bone but rather particles encapsulated by connectivetissue in the HA-treated sites. Moreover, at the time ofbiopsy (6 to 8 months) almost all of the bioglass parti-cles were absorbed and replaced by newly formed bone.

Although more vital bone was evident in our studyin the BG-treated sockets compared to both theDFDBA-treated and ungrafted sockets, the critical ques-tion remains as to whether this bone can support animplant. Schepers et al.39 studied the efficacy of usingbioactive glass in the treatment of bone defects priorto implant placement. Defects were created in themandible of 6 beagle dogs by removing the intra-alve-olar septa. One side was filled with BG particles and theother side was left empty. After 4 months of healing, 3implants 10 mm in length and 3.3 mm in diameter wereplaced in the BG-treated (test) area and untreated (con-trol) areas. In 3 dogs the unloaded implants were biop-sied at 3 months while in the other 3 dogs the implantswere functionally loaded with fixed partial prosthesisfor 7 weeks before sacrifice. Implants placed in BGtreated sites showed 52.1% more interfacial bone thanthose in the control sites. At a distance of 3 mm fromthe implant surface 134.7% more bone tissue was foundin the test compared to the control sites. Thus theauthors concluded that not only did BG not interferewith implant healing but actually improved the quan-tity of bone at the implant/bone interface. The healingresponse of BG-treated sockets in the above study aswell as in the present paper differs from that reportedby Becker et al. utilizing DFDBA, mineralized freeze-dried bone allograft (MFDBA), and autogenous bone forsocket fill.22 Becker et al. utilized 4- to 13-month post-surgical biopsies and reported that the "over-riding his-tologic characteristic of sites implanted with DFDBAor MFDBA was retention of non-vital graft particleswithin fibrous connective tissue." They concluded thatautologous intraoral bone chips and the allografts ". . .may serve as biologic fillers." In another study, Beckeret al .2 3 placed microscrews into extraction socketstreated with xenogenic bovine bone, DFDBA, or intra-oral autologous bone. Biopsies from the bovine boneand DFDBA implanted sockets revealed dead particlesentrapped within dense connective tissue. They con-cluded that neither xenogenic bovine bone, DFDBA,

nor autogenous bone "contribute to bone to micro screwcontact and are not recommended for enhancement ofvital bone to implant contacts."23

Although intrastudy comparisons of materials mustbe approached cautiously, differences in the propertiesof BG, a different model system, complete soft tissuecoverage of the materials, and a more standard heal-ing time may account for the improved results seen inthe present study.

Lastly, it is of interest to note that in the presentstudy DFDBA-treated sockets presented similar lev-els of vital bone 6 to 8 months postgrafting comparedto the ungrafted controls. The factors mentioned pre-viously regarding the surgical technique and healingtimes employed may again account for the betterresponse obtained here with DFDBA than in previousstudies.2223 A 1999 histomorphometric study com-paring unfilled extraction sockets with those filled withDFDBA and covered with expanded polytetrafluoro-ethyiene membranes at 8 to 23 months postgraftingfound similar levels of trabecular bone in both sock-ets.30 However, in the present study, since the vitalbone values were only slightly higher than that foundwith the ungrafted sockets, DFDBA would have ques-tionable value when utilized in extraction socket treat-ment.

CONCLUSIONSThis pnot study attempted to develop t: •Huiblo huna imodel to histologically evaluate various materials uti-lized for treatment of extraction sockets. This paperdescribes the materials and technique utilized to accom-plish that goal. In a test of 30 extraction sockets treatedwith a bioactive glass of limited particle size (BG), de-mineralized freeze-dried bone (DFDBA), or debridementonly (C), BG-treated sockets yielded more vital bone(59.5%) in 6- to 8-month healing biopsies than eitherDFDBA or C. Similar levels of vital bone were observedwith DFDBA- (34.7%) and C-treated sockets (32,4%).These differences, however, were not statistically sig-nificant. Further studies with greater numbers of sitesare indicated to determine if the increased vital bonefound in BG-treated sockets translates into moreimplant/bone contact in humans as has been shown tobe the case in an animal model. However, the presentstudy demonstrated that BG is an osteoconductive bonereplacement material and, although the difference invital bone was not statistically significant among the 3treatment groups, BG has a positive effect on sockethealing at 6 to 8 months postextraction.

ACKNOWLEDGMENTSThe authors acknowledge the contributions of HariPrasad for his assistance with the histologic prepara-tion and histomorphometric analysis. The authorswould also like to thank Dr. Martha Nunn, Goldman

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Extraction Socket Healing After Implants With Bioactive Glass or DFDB Aliograft Volume 73 • Number I

School of Dental Medicine at Boston University, for herhelp with the preparation and analysis of the statisticsfor the study. The study was supported by a grant fromOrthovita. Malvern, Pennsylvania.

REFERENCES

1. Branemark P-I, Hansson BO. Adell R, et al. Osseointe-grated implants in the treatment of the edentulous jaw.Experience from a 10-year period. Scand J Ptast ReconstrSurg 1977-.I l(Suppl. 16):39-94.

2. Branemark P. Ten-year survival rates of fixed prostheses on four or six implants ad modum Branemark in fulledentulism. Clin Oral Implants Res 1995;6:227-231.

3. Lekholm <J. Gunne J, Henry P, et al. Survival of theBranemark implant in partially edentulous jaws: A 10-year prospective multicenter study. Int J Oral MaxiliofacImplants 1999:14:639-645.

4. Lekholm (J, van Steenberghe D, Hermann I, et al.Osseointegration implants in the treatment of partiallyedentulous jaws: A prospective 5-year multicenter study.frif J Oral MaxlUafac Implants 1994:9:627-635.

5. Mellonig J, Tripplett, RG. Guided tissue regeneration andendosseous dental implants. Int J Periodontics Restora-tive Dent 1993:13:108-119.

6. Simion M, Dahlin C, Trisi D, Piattelli A. Qualitative andquantitative comparative study on different filling mate-rials used in bone tissue regeneration: A controlled clin-ical study. Int J Periodontics Restorative Dent 1994; 14:199-215.

7. Simion M, Trisi P, Piattelli A. Vertical ridge augmentationusing a membrane technique associated with osseoin-tegrated implants. Int J Periodontics Restorative Dent1994:14:496-51 1.

8. Gross JS. Bone grafting materials for dental applica-tions: A practical guide. Compend Contin Educ Dent1997:18:1013-1024.

9. Nevins M, Mellonig JT. Clem DR III, Reiser GM, Buser DA.Implants in regenerated bone: Long-term survival. Int JPeriodontics Restorative Dent 1998:18:35-45.

10. Fugazzotto PA. Success and failure rates of osseointe-grated implants in function in regenerated bone for 6 to51 months: A preliminary report. Int J Oral MaxitlofacImplants 1997:12:17-24.

I 1. Buser D, Dula K, Lang MP, Nyman S. Long-term stabil-ity of osseointegrated implants in bone regenerated withthe membrane technique: 5 year results of a prospec-tive study with 12 implants. Clin Oral Implants Res1996:7:175-183.

12. Carlsson GE, Thilander H. Hedegard B. Histologicchanges in the upper alveolar process after extractionwith or without insertion of an immediate full denture.Ada Odontot Scand 1967:25:21-43.

I 3. Ashman A, Bruins P. Prevention of alveolar bone losspost-extraction with HTR grafting material. Implantol1987:13:270-281.

14. Lekovic V, Kenney EB, Weinlaender M, et al. A boneregenerative approach to alveolar ridge maintenancefollowing tooth extraction. Report of 10 cases. J Peri-odontol 1997:68:563-570.

15. Lekovic V, Camargo P, Klokkevold P, Weinlaender M.Preservation of alveolar bone in extraction sockets usingbioabsorbable membranes. J Periodontol 1998:69:1044-1049.

16. Nemcovsky CE, Serfaty V. Alveolar ridge preservationfollowing tooth extraction of maxillary anterior teeth.Report on 23 consecutive cases. J Periodontol 1996;67:390-395.

17. Johnson K. A study of dimensional changes occurringin the maxilla following tooth extraction. Aust ProsthelJ 1969:14:241-244.

18. Johnson K. A study of dimensional changes occurringin the maxilla following closed face immediate denturetreatment. Aust Prosthet J 1969:14:371-376.

19. Abrams H. Kopczyk RA, Kaplan A. Incidence of ante-rior ridge deformities in partially edentulous patients.J Prosthel Dent 1987:57:191-194.

20. Froum S, Orlowski W. Ridge preservation utilizing analloplast prior to implant placement: Clinical and histo-logical case reports. Practical Periodontics Acsthet Dent2000:12:393-402.

21. Artzi Z, Tal H, Dayan D. Porous bovine bone mineral inhealing of human extraction sockets. Part 1: Histomor-phometric evaluations at 9 months. J Periodontol2000:71: 1015-1023.

22. Becker W, (Jrist M, Becker B, et al. Clinical and histologic observations of sites implanted with intraoral autol-ogous bone grafts or allografts. 15 human case reports.J Periodontol 1996;67:1025-1033.

23. Becker W, Clokie C, Sennerby L. Grist MR, Becker BE.Histologic findings after implantation and evaluation ofdifferent grafting materials and titanium micro screwsinto extraction sockets: Case reports. J Pcriodonto! 1998;69:414-421.

24. Froum SJ. Tarnow DP. Wallace SS, Rohrer MD, Cho SC.Sinus floor elevation using anorganic bovine bone matrix(OsteoGraf/N) with and without autogenous bone: Aclinical, histologic, radiographic. and histomorphomet-ric analysis—Part 2 of an ongoing prospective study. IntJ Periodontics Restorative Dent 1998; 18:528-543.

25. Amler MG, Johnson PL, Salmon L. Histological and his-tochemical investigation of human alveolar socket heal-ing in undisturbed extraction wound. J Am Dent Assoc1960:61:32-44.

26. Schepers E, De Clercq M, Ducheyne P, Kempeneers R.Bioactive glass paniculate material as a filler for bonelesions. J Oral Rehabil 1991; 18:439 452.

27. Furusawa T, Mizunuma K. Osteoconductive propertiesand resorbable bioactive glass as a bone-grafting mate-rial. Implant Dent 1997;62:93-101.

28. Cancian DC, Hochuli-Vieira E, Marcantonio RA, Mar-cantonio E Jr. Use of BioGran and Calcitite in bonedefects: Histologic study in monkeys (Cebus apella). IntJ Oral Maxiliofac Implants 1999; 14:859-864.

29. Schepers E, Barbier L, Ducheyne P. Implant placementenhanced by bioactive glass particles of narrow sizerange. Int J Oral Maxitlofac Implants 1998; 13:655-665.

30. Smukler H, Landi L, Setayesh R. Histomorphometricevaluation of extraction sockets and deficient alveolarridges with aliograft and barrier membrane: A pilot study.Int J Oral Maxiliofac Implants 1999:14:407-416.

Send reprint requests to: Dr. Stuart Froum, 17 West 54thSt., New York. MY 10019. Fax: 212/246-7599; e-mail: [email protected].

Accepted for publication June 29. 2001.

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