Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft: a...

Review

Maxillary sinus floor augmentation withBio-Oss or Bio-Oss mixed withautogenous bone as graft: a systematicreview

Thomas JensenS�ren SchouAndreas StavropoulosHendrik TerheydenPalle Holmstrup

Authors’ affiliations:Thomas Jensen, Department of Oral and MaxillofacialSurgery, Aalborg Hospital, Aarhus University Hospital,Aalborg, DenmarkS�ren Schou, Department of Oral and MaxillofacialSurgery and Oral Pathology, School of Dentistry,University of Aarhus, Aarhus, DenmarkAndreas Stavropoulos, Palle Holmstrup, Department ofPeriodontology, School of Dentistry, University ofAarhus, Aarhus, DenmarkHendrik Terheyden, Department of Oral andMaxillofacial Surgery, Red Cross Hospital Kassel,Kassel, GermanyPalle Holmstrup, Department of Periodontology,School of Dentistry, University of Copenhagen,Copenhagen, Denmark

Corresponding author:Dr Thomas JensenDepartment of Oral and Maxillofacial SurgeryAalborg Hospital, Aarhus University Hospital18-22 HobrovejDK-9000 AalborgDenmarkTel.:þ45 99 32 28 00Fax:þ 45 99 32 28 05e-mail: [email protected]

Key words: alveolar ridge augmentation, bone substitutes, bone transplantation, dental im-

plants, maxillary sinus, oral implants, systematic review

Abstract

Aims: The objective of the present systematic review was to test the hypothesis of no differences in

the implant treatment outcome when Bio-Oss or Bio-Oss mixed with autogenous bone is used as graft

for the maxillary sinus floor augmentation (MSFA) applying the lateral window technique.

Material and methods: A MEDLINE (PubMed) search in combination with a hand search of relevant

journals was conducted by including human studies published in English from January 1, 1990 to June

1, 2010. The search provided 879 titles and 35 studies fulfilled the inclusion criteria. Considerable

variation in the included studies prevented meta-analysis from being performed and no long-term

study comparing MSFA with the two treatment modalities was identified. Also, the survival of

suprastructures after the two augmentation procedures was not compared within the same study.

Results: The 1-year implant survival was compared in one study demonstrating no statistically significant

difference. The implant survival was 96% with Bio-Oss and 94% with a mixture of 80% Bio-Oss and 20%

autogenous mandibular bone. Addition of a limited amount of autogenous bone to Bio-Oss seemed not

to increase the amount of new bone formation and bone-to-implant contact compared with Bio-Oss.

Conclusions: Therefore, the hypothesis of no differences between the use of Bio-Oss or Bio-Oss mixed

with autogenous bone as graft for MSFA could neither be confirmed nor rejected.

The maxillary sinus floor augmentation (MSFA)

is the most frequently used method to increase

the alveolar bone height of the posterior part of the

maxilla, and the treatment outcome has been

reported in recently published systematic reviews

(Wallace & Froum 2003; Del Fabbro et al. 2004;

Esposito et al. 2006; Browaeys et al. 2007; Pje-

tursson et al. 2008; Chiapasco et al. 2009; Jensen

& Terheyden 2009; Nkenke & Stelzle 2009).

Autogenous bone is generally the preferred graft

(Burchardt 1983), and oral implants inserted in

sinuses augmented with autogenous bone have

demonstrated high survival rates as documented

in several reviews (Tong et al. 1998; Wallace &

Froum 2003; Del Fabbro et al. 2004; Esposito et

al. 2006; Pjetursson et al. 2008; Chiapasco et al.

2009; Jensen & Terheyden 2009; Nkenke &

Stelzle 2009). However, the use of autogenous

bone grafts is associated with the risk of donor site

morbidity and unpredictable graft resorption (Jo-

hansson et al. 2001; Clavero & Lundgren 2003;

Cricchio & Lundgren 2003; Wiltfang et al. 2005;

Zizelmann et al. 2007; Nkenke & Stelzle 2009).

A bone substitute of bovine origin (Bio-Oss,

Geistlich Pharma, Wolhusen, Switzerland) is

frequently used for various augmentation proce-

dures, either alone or in combination with auto-

genous bone (Wallace & Froum 2003; Del Fabbro

et al. 2004; Esposito et al. 2006; Browaeys et al.

2007; Pjetursson et al. 2008; Chiapasco et al.

2009; Jensen & Terheyden 2009; Nkenke &

Stelzle 2009). It could from a biological point of

view be an advantage to mix Bio-Oss and auto-

genous bone due to the osteoinductive properties

of autogenous bone (Bosshardt & Schenk 2009).

However, it was concluded in a recently pub-

lished systematic review that the amount of new

bone formation was comparable when Bio-Oss or

Bio-Oss mixed with autogenous bone was used as

graft material for MSFA (Handschel et al. 2009)

but the clinical outcome of implant treatment

involving MSFA with Bio-Oss or Bio-Oss mixed

with autogenous bone in humans has not been

assessed specifically in a systematic review.

Objective

The objective of the present systematic review

was to test the hypothesis of no differences in the

Date:Accepted 9 January 2011

To cite this article:Jensen T, Schou S, Stavropoulos A, Terheyden H,Holmstrup P. Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft: asystematic review.

Clin. Oral Impl. Res. 23, 2012;263–273doi: 10.1111/j.1600-0501.2011.02168.x

© 2011 John Wiley & Sons A/S 263

implant treatment outcome when Bio-Oss or

Bio-Oss mixed with autogenous bone is used as

graft for the MSFA applying the lateral window

technique.

Criteria for considering studies forthis review

Types of studies, participants, and intervention

Human studies evaluating MSFA with Bio-Oss

or Bio-Oss mixed with autogenous bone applying

the lateral window technique were assessed.

Types of outcome measures

The primary outcome measures included:

� Survival of suprastructures. Loss of supras-

tructure was defined as a total loss because of

a mechanical and/or biological complication.

� Survival of implants. Loss of implants was

defined as mobility of previously clinically

osseointegrated implants and removal of

non-mobile implants due to progressive peri-

implant marginal bone loss and infection.

Moreover, the following secondary outcome

measures were assessed:

� Bone regeneration.

� Bone-to-implant contact (BIC) and biomecha-

nical test values, experimental implants.

� Biodegradation of Bio-Oss.

� Volumetric stability of the graft.

� Postoperative complications, augmented

region.

Search strategy for identification of studies

The search strategy used for identification of

studies is summarized in Fig. 1. A MEDLINE

(PubMed) search was conducted by including

studies published in English from January 1,

1990 to June 1, 2010. The search strategy uti-

lized a combination of controlled vocabulary

(MeSH) and free text terms:

1. exp Maxillary sinus.

2. exp Bone regeneration.

3. ‘‘Bio-Oss’’.

4. 1 AND 2 OR 3.

The search was supplemented by a thorough

hand-search page by page of relevant journals

(Fig. 1). The manual search also included the

bibliographies of all articles selected for full-text

screening as well as previously published reviews

relevant for the present systematic review. The

search was performed by one reviewer (T. J.).

Methods of the review

Study selection

The titles of the identified reports were initially

screened. The abstract was assessed when the

title indicated that the study fulfilled the inclu-

sion criteria. Full-text analysis was carried out

when the abstract was unavailable or when the

abstract indicated that the inclusion criteria were

fulfilled. The study selection was performed by

one reviewer (T. J.).

Inclusion criteria

Studies assessing the outcome of MSFA with Bio-

Oss or Bio-Oss mixed with autogenous bone as

graft were included by addressing the previously

described outcome measures. The review exclu-

sively focused on studies applying the lateral

window technique for the MSFA. In addition, at

least 10 patients should be included in the study,

and the treatment should involve osseointegrated

oral implants. The survival of the suprastructures

as well as the implants after a loading period of

more than 1 year was addressed. Studies compar-

ing Bio-Oss with other bone substitutes were

included, if the outcome measures could be

identified for Bio-Oss or Bio-Oss mixed with

autogenous bone, while reports on Bio-Oss

mixed with other bone substitutes or platelet-

rich plasma were excluded. Also, studies with

insufficient description of the performed num-

bers of MSFA procedures and numbers of inserted

implants were excluded.

Quality assessment

The quality assessment of the included studies

was undertaken by one review author (T. J.) as

part of the data extraction process. The quality

assessment was performed according to the fol-

lowing parameters:

� Adequate randomization (yes/no).

� Blinding of outcome assessment (yes/no).

� Completeness of follow-up. A clear explana-

tion for withdrawals and drop-outs (yes/no).

� Histologic evaluation involving unbiased

stereologic methods (Gundersen et al.

1988a, 1988b) (yes/no).

The studies were grouped according to:

� Low risk of bias (plausible bias unlikely to

seriously alter the results) if all above-de-

scribed quality criteria were met.

� High risk of bias (plausible bias that seriously

weakens confidence in the results) if all

above-described quality criteria were not met.

Data extraction

Data were extracted by one reviewer (T. J.)

according to the data collection form ensuring

systematic recording of the outcome measures.

In addition, relevant characteristics of the study

were recorded.

Data synthesis

The studies included revealed considerable varia-

tions in design, i.e. the alveolar bone height

before MSFA, type of Bio-Oss (particles or

blocks), ratio of Bio-Oss and autogenous bone,

type of suprastructure and implant, immediate or

delayed implant placement, presence or absence

of a barrier membrane, length of observation

period, and type of outcome measures. Therefore,

meta-analyses were not applicable.

Description of studies

The search result is outlined in Fig. 1. A total of

879 titles were identified and 173 abstracts were

reviewed. Full-text analysis included 68 articles

and 35 studies were finally included in the re-

view (Piattelli et al. 1999; Maiorana et al. 2000;

Valentini et al. 2000; Yildirim et al. 2000; Hall-

man et al. 2001a, 2001b; Tawil & Mawla 2001;

Number

879Medline (PubMed) search

173Abstracts reviewed:

68Articles reviewed:

35Articles included:

Hand-searched journals (1990-2010):

Clin Implant Dent Relat Res (1999-2010)Clin Oral Implants Res

European Journal of Oral Implantology(2008-2010)

Int J Oral Maxillofacial Implants Int J Oral Maxillofacial Surg

Int J Periodontics Restorative DentJ Oral Maxillofacial Surg

(0)

Fig. 1. Search strategy used for identification of studies.

Jensen et al �Maxillary sinus floor augmentation

264 | Clin. Oral Impl. Res. 23, 2012 / 263–273 © 2011 John Wiley & Sons A/S

Yildirim et al. 2001; Artzi et al. 2002; Hallman

et al. 2002a, 2002b; Fugazzotto 2003; Valentini

& Abensur 2003; Hallman & Nordin 2004;

Hallman & Zetterqvist 2004; Hatano et al.

2004; John & Wenz 2004; Orsini et al. 2005;

Degidi et al. 2006; Froum et al. 2006; Lee et al.

2006; Mangano et al. 2007; Marchetti et al.

2007; Mardinger et al. 2007; Cordaro et al.

2008; Froum et al. 2008; Simunek et al. 2008;

Cannizzaro et al. 2009; Ferreira et al. 2009; Kim

et al. 2009; Lindgren et al. 2009; de Vicente et al.

2010; Galindo-Moreno et al. 2010a, 2010b; Lam-

bert et al. 2010). No article was included as the

result of hand searching.

Comparative studies have focused on implant

survival (Hallman et al. 2002a), bone regenera-

tion (Hallman et al. 2002a; John & Wenz 2004;

Simunek et al. 2008), BIC (Hallman et al. 2002a),

biodegradation of Bio-Oss (Hallman et al. 2002a),

and postoperative complications (John & Wenz

2004). One study was not included (Hallman et

al. 2005), because the same patient sample with a

5-year observation period was reported in another

publication (Hallman & Zetterqvist 2004). The

main results are described below and summarized

in Tables 1–3.

Methodological quality

The quality of the included studies is summar-

ized in Table 4. All studies assessing Bio-Oss or

Bio-Oss mixed with autogenous bone were con-

sidered at high risk of bias. In studies with

randomization, the randomization procedure

was inadequate. In addition, blinding of outcome

assessment, clear explanation of withdrawals and

drop-outs, and histologic evaluation involving

unbiased stereologic methods were not included.

Results

Below for each outcome measure, results of

comparative studies of Bio-Oss as opposed to

Bio-Oss mixed with autogenous bone are pre-

sented first (Table 1). This is followed by results

of studies including solely one of the two treat-

ment modalities (Supplementary studies, Tables

2 and 3). For each outcome measure, a summary

is finally provided.

Primary outcome measures

Survival of suprastructures

Comparative studies. No study was identified.

Supplementary studies. The survival of supras-

tructures was 100% after 2–6 years when Bio-

Oss was used (Lambert et al. 2010).

The 5-year survival of the suprastructures has

been reported in one study using a mixture of

80% Bio-Oss and 20% autogenous bone (Hall-

man & Zetterqvist 2004). All patients were

rehabilitated with fixed dental prostheses. After

5 years of loading, one small dental prosthesis

was transformed into a single crown in one

patient. The other bridges were still in function

giving a survival of 95%. Moreover, no supras-

tructure failed after 1 year of loading when Bio-

Oss was mixed with small volumes of autoge-

nous bone from the maxillary tuberosity (Kim

et al. 2009).

Summary. The survival of the suprastructures

after MSFA with the two treatment modalities

has never been compared within the same study.

Survival of implants

Comparative studies. The survival of implants

after MSFA with Bio-Oss or a mixture of 80%

Bio-Oss and 20% autogenous mandibular bone

has been compared in one study demonstrating

no statistically significant differences (Hallman

et al. 2002a). The 1-year implant survival was

96% with Bio-Oss and 94% with mixed Bio-Oss

and autogenous bone.

Supplementary studies. The implant survival

varied between 70% and 100% for simulta-

neously inserted implants, and 94% and 100%

for delayed inserted implants after 14–60 months

when Bio-Oss was used (Valentini et al. 2000;

Tawil & Mawla 2001; Hallman et al. 2002b;

Valentini & Abensur 2003; Hallman & Nordin

2004; Mangano et al. 2007; Mardinger et al.

2007; Ferreira et al. 2009; Lambert et al. 2010).

The 5-year implant survival was 89% for

implants inserted 6 months after MSFA with a

mixture of 80% Bio-Oss and 20% autogenous

mandibular bone (Hallman & Zetterqvist 2004).

The 5-year implant survival was 88% for simul-

taneously inserted implants and 97% for delayed

Table 1. Comparative studies

Patient Material and methods Length ofobservationperiod

Outcome measures Reference

Primary Secondary

10 14 sinuses with Bio-Oss43 Branemark implants after 8.5months14 test implants after 8.5 months

12–15 months Suprastructure:NRImplant: 96%

BIC Bone ResidualBio-Oss

PC:NR

Hallman et al.(2002a)

32% 42% 12%

11 11 sinuses with 80% Bio-Oss and20% ramus bone35 Branemark after 6.5 months11 test implants after 6.5 months

1 year Suprastructure:NRImplant: 94%

54% 40% 12%

21 21 sinuses with Bio-Oss11 biopsies after 3–5 months10 biopsies after 6–8 months

3–8 months Suprastructure:NRImplant: NR

NFB Residual Bio-Oss PC:None

John & Wenz(2004)3–5 months 6–8 months 3–5 months 6–8

months25% 35% 15% 15%

13 13 sinuses with 66% Bio-Oss and33% chin bone8 biopsies after 3–5 months5 biopsies after 6–8 months

28% 39% 21% 13%

10 10 sinuses with Bio-Oss10 biopsies after 9 months

9 months Suprastructure:NRImplant: NR

NFB Connectivetissue

Residual Bio-Oss PC:NR

Simunek et al.(2008)

34% 35% 31%10 10 sinuses with 80% to 90% Bio-Oss

and 10% to 20% bone fromtuberosity10 biopsies after 9 months

24% 42% 33%

All group values referred to are expressed as mean values.

NFB, newly formed bone; BIC, bone-to-implant contact; NR, not reported; PC, postoperative complications.


© 2011 John Wiley & Sons A/S 265 | Clin. Oral Impl. Res. 23, 2012 / 263–273

Tab

le2.

Su

pp

lem

en

tary

stu

die

sw

ith

Bio

-Oss

Pati

en

tM

ate

rial

an

dm

eth

od

sLe

ng

tho

fo

bse

rvati

on

peri

od

Ou

tco

me

measu

res

Refe

ren

ce

Pri

mary

Seco

nd

ary

20

20

sin

use

sw

ith

Bio

-Oss

20

bio

psi

es

retr

ieve

daft

er

6–4

8m

on

ths

6,

9,

18,

an

d48

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:N

R6

an

d9

mo

nth

s18

an

d48

mo

nth

sPC

:N

RPia

ttell

iet

al.

(1999)

Mo

stB

io-O

sssu

rro

un

ded

by

NFB

Bio

-Oss

easi

lyre

cog

niz

ed

15

20

sin

use

sw

ith

Bio

-Oss

57

Fria

tec

imp

lan

tsaft

er

6m

on

ths

3b

iop

sies

3.2

–4.8

years

Sup

rast

ruct

ure

:N

RIm

pla

nt:

98

%6

mo

nth

s12

mo

nth

sPC

:G

raft

fail

ure

du

eto

infe

ctio

n:

5%

Vale

nti

ni

et

al.

(2000)

NFB

21%

28%

Bio

-Oss

39%

27%

Bo

ne

marr

ow

40%

45%

11

15

sin

use

sw

ith

Bio

-Oss

38

Bra

nem

ark

imp

lan

tsaft

er

7m

on

ths

22

bio

psi

es

aft

er

7m

on

ths

7m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

90

%N

FBR

esi

du

al

Bio

-Oss

PC

:N

ose

ble

ed

ing

:20%

Yil

dir

imet

al.

(2000)

15%

30%

29

15

sin

use

sw

ith

Bio

-Oss

an

dB

io-G

ide

mem

bra

ne

18

Bra

nem

ark

imp

lan

tssi

mu

ltan

eo

usl

y11

Bra

nem

ark

imp

lan

tsaft

er

6–9

mo

nth

s

12–4

0m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt,

sim

ult

an

eo

usl

y:94%

Imp

lan

t,d

ela

yed

:91%

NR

PC

:N

on

eTa

wil

&M

aw

la(2

001)

15

sin

use

sw

ith

Bio

-Oss

wit

ho

ut

Bio

-Gid

em

em

bra

ne

23

Bra

nem

ark

imp

lan

tssi

mu

ltan

eo

usl

y9

Bra

nem

ark

imp

lan

tsaft

er

6–9

mo

nth

s

Sup

rast

ruct

ure

:N

RIm

pla

nt,

sim

ult

an

eo

usl

y:70%

Imp

lan

t,d

ela

yed

:100%

10

10

sin

use

sw

ith

Bio

-Oss

36

Steri

-Oss

imp

lan

tssi

mu

ltan

eo

usl

y10

bio

psi

es

1ye

ar

Sup

rast

ruct

ure

:N

RIm

pla

nt:

100%

Late

ral

part

of

gra

ft:

34%

bo

ne

Cen

tral

part

of

gra

ft:

53%

bo

ne

PC

:N

on

eA

rtzi

et

al.

(2002)

NR

31

sin

use

sw

ith

Bio

-Oss

No

.o

fim

pla

nts

:N

R31

bio

psi

es

aft

er

3–1

3m

on

ths

3–1

3m

on

ths

NR

No

.o

fm

on

ths

3–4

5–6

8–9

12–1

3PC

:N

RFu

gazz

ott

o(2

003)

No

.o

fb

iop

sies

39

14

5R

esi

du

al

Bio

-Oss

60%

21%

11%

0%

Bo

ne

19%

40%

68%

69%

39

13

sin

use

sw

ith

Bio

-Oss

4IM

Z&

23

Bra

nem

ark

imp

lan

tssi

mu

ltan

eo

usl

y

5ye

ars

Sup

rast

ruct

ure

:N

RIm

pla

nt,

IMZ:

100%

Imp

lan

t,B

ran

em

ark

:91%

NR

PC

:Si

nu

sin

fect

ion

:3%

Vale

nti

ni

&A

ben

sur

(2003)

37

sin

use

sw

ith

Bio

-Oss

79

IMZ

&21

Bra

nem

ark

imp

lan

tsaft

er

6m

on

ths

6ye

ars

Sup

rast

ruct

ure

:N

RIm

pla

nt,

IMZ:

99%

Imp

lan

t,B

ran

em

ark

:95%

50

71

sin

use

sw

ith

Bio

-Oss

196

ITI

imp

lan

tsaft

er

8m

on

ths

20

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:96%

NR

PC

:In

fect

ion

:3%

Hall

man

&N

ord

in(2

004)

12

18

sin

use

sw

ith

Bio

-Oss

No

.o

fim

pla

nts

:N

R18

bio

psi

es

aft

er

6m

on

ths

6m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

96%

Lig

ht

mic

rosc

op

ySc

an

nin

gele

ctro

nm

icro

-sc

op

y

Tran

smis

-si

on

ele

ctro

nm

icro

-sc

op

y

PC

:N

RO

rsin

iet

al.

(2005)

Bio

-Oss

surr

ou

nd

ed

by

NFB

Bo

ne

ad

here

nt

toB

io-O

ss

Bio

-Oss

surr

ou

n-

ded

by

NFB

20

10

sin

use

sw

ith

Bio

-Oss

10

bio

psi

es

aft

er

3m

on

ths

3an

d6

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:N

RM

icro

vess

el

den

sity

En

do

the-

lial

gro

wth

fact

or

NFB

Resi

du

al-

Bio

-Oss

PC

:N

RD

eg

idi

et

al.

(2006)

NFB

MB

NFB

MB

12%

35%

32n

10n

85%

40%

10

sin

use

sw

ith

Bio

-Oss

10

bio

psi

es

aft

er

6m

on

ths

35n

21n

65%

30%

35%

30%



inserted implants with a mixture of 30% Bio-Oss

and 70% autogenous mandibular or iliac bone

(Marchetti et al. 2007). The 2-year implant

survival was 100% for implants inserted after 6

months in sinuses augmented with 50% Bio-Oss

and 50% autogenous bone from the lateral max-

illary wall (Galindo-Moreno et al. 2010b), and

the 1-year implant survival was 89% for simul-

taneously inserted implants in sinuses augmen-

ted with 50% Bio-Oss and 50% tuberosity bone

(Cannizzaro et al. 2009).

Summary. The 1-year implant survival after

MSFA with the two treatment modalities was

only compared in one study demonstrating an

implant survival of 96% with Bio-Oss and 94%

with a mixture of 80% Bio-Oss and 20% auto-

genous mandibular bone.

Secondary outcome measures

Bone regeneration

Comparative studies. Assessment of bone regen-

eration after MSFA with Bio-Oss or Bio-Oss

mixed with autogenous bone revealed a bone

area of 42% for Bio-Oss after 15 months and

40% for a mixture of 80% Bio-Oss and 20%

autogenous bone after 13 months (Hallman et al.

2002a). Biopsies obtained 9 months after MSFA

with Bio-Oss or Bio-Oss mixed with 10–20%

tuberosity bone revealed 34% and 24% newly

formed bone, respectively (Simunek et al. 2008).

Biopsies obtained after MSFA with Bio-Oss

showed 25% newly formed bone after 3–5

months and 35% after 6–8 months. The corre-

sponding figures for a mixture of 66% Bio-Oss

and 33% autogenous bone were 28% and 39%,

respectively (John & Wenz 2004). In all studies,

no statistically significant differences in bone

regeneration were found between the two treat-

ment modalities.

Supplementary studies. The proportion of newly

formed bone varied from 12% to 69% after 3–12

months when Bio-Oss was used (Valentini et al.

2000; Yildirim et al. 2000; Fugazzotto 2003;

Degidi et al. 2006; Froum et al. 2006; Lee et al.

2006; Mangano et al. 2007; Cordaro et al. 2008;

Froum et al. 2008; Lindgren et al. 2009). The

Bio-Oss particles were incorporated in newly

formed bone, and the proportion of newly formed

bone seemed to increase with the length of the

observation period. However, comparable miner-

alization was reported 18 months and 4 years

after MSFA (Piattelli et al. 1999).

Newly formed bone was identified after MSFA

with Bio-Oss mixed with autogenous bone

(Maiorana et al. 2000; Hallman et al. 2001a;

Yildirim et al. 2001; de Vicente et al. 2010;

13

13

sin

use

sw

ith

Bio

-Oss

9b

iop

sies

aft

er

26–3

0w

eeks

26–3

0w

eeks

Sup

rast

ruct

ure

:N

RIm

pla

nt:

NR

Vit

al

bo

ne

Bo

ne

marr

ow

Resi

du

al

Bio

-Oss

PC

:N

RFr

ou

met

al.

(2006)

12%

55%

33%

10

11

sin

use

sw

ith

Bio

-Oss

30

Rest

ore

RB

Mim

pla

nts

aft

er

6m

on

ths

14

bio

psi

es

aft

er

6&

12

mo

nth

s

12

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:100%

NFB

6m

on

ths

12

mo

nth

sPC

:N

ose

ble

ed

ing

:33%

Lee

et

al.

(2006)

18%

27%

Resi

du

al

Bio

-Oss

30%

29%

Soft

tiss

ue

52%

45%

Bo

ne–B

io-O

ssco

nta

ct32%

42%

20

No

.o

fsi

nu

ses:

NR

50

Led

er

imp

lan

tssi

mu

ltan

eo

usl

y25

bio

psi

es

aft

er

6m

on

ths

1ye

ar

Sup

rast

ruct

ure

:N

RIm

pla

nt:

96%

NFB

Bo

ne

marr

ow

Resi

du

al

Bio

-Oss

PC

:N

on

eM

an

gan

oet

al.

(2007)

36%

25%

39%

55

60

sin

use

sw

ith

Bio

-Oss

164

Steri

oss

,Zim

mer,

MIS

imp

lan

tssi

mu

ltan

eo

usl

y

16–6

6m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

95%

NR

PC

:A

cute

sin

usi

tis:

5%

Mard

ing

er

et

al.

(2007)

No

.o

fp

ati

en

ts:

NR

23

sin

use

sw

ith

Bio

-Oss

55

imp

lan

tsaft

er

180–2

40

days

18

bio

psi

es

aft

er

180–2

40

days

180–2

40

days

Sup

rast

ruct

ure

:N

RIm

pla

nt:

NR

NFB

Co

nn

ec-

tive

tiss

ue

Resi

du

al

Bio

-Oss

PC

:N

RC

ord

aro

et

al.

(2008)

20%

43%

38%

12

12

sin

use

sw

ith

Bio

-Oss

11

bio

psi

es

aft

er

6–8

mo

nth

s6–8

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:N

RV

ital

bo

ne

Bo

ne

marr

ow

Resi

du

al

Bio

-Oss

PC

:N

RFr

ou

met

al.

(2008)

22%

52%

26%

314

406

sin

use

sw

ith

Bio

-Oss

118

Bra

nem

ark

,3i,

Oss

eo

tite

imp

lan

tssi

mu

ltan

eo

usl

y907

Bra

nem

ark

,3i,

Oss

eo

tite

imp

lan

tsaft

er

6–1

2m

on

ths

7b

iop

sies

aft

er

10–1

2m

on

ths

3ye

ars

Sup

rast

ruct

ure

:N

RIm

pla

nt,

sim

ult

an

eo

usl

y:97%

Imp

lan

t,d

ela

yed

:98%

NFB

Bo

ne

marr

ow

Resi

du

al

Bio

-Oss

PC

:In

fect

ion

:1%

Gra

ftre

mo

val:

0.5

%

Ferr

eir

aet

al.

(2009)

39%

53%

8%

11

11

sin

use

sw

ith

Bio

-Oss

11

test

imp

lan

tssi

mu

ltan

eo

usl

y11

bio

psi

es

aft

er

8m

on

ths

8m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

NR

NFB

BIC

Resi

du

al

Bio

-Oss

PC

:N

on

eLi

nd

gre

net

al.

(2009)

42%

55%

12%

40

50

sin

use

sw

ith

Bio

-Oss

102

Rep

lace

,B

ran

em

ark

,St

rau

man

nim

pla

nts

sim

ult

an

eo

usl

y

2–6

years

Sup

rast

ruct

ure

:100%

Imp

lan

t:98%

NR

PC

:N

on

eLa

mb

ert

et

al.

(2010)

nN

um

ber

of

mic

rove

ssels

per

squ

are

mil

lim

ete

r.

All

gro

up

valu

es

refe

rred

toare

exp

ress

ed

as

mean

valu

es.

BIC

,b

on

e-t

o-i

mp

lan

tco

nta

ct;

MB

,m

atu

reb

on

e;

NFB

,n

ew

lyfo

rmed

bo

ne;

NR

,n

ot

rep

ort

ed

;PC

,p

ost

op

era

tive

com

pli

cati

on

s.



Tab

le3.

Su

pp

lem

en

tary

stu

die

sw

ith

Bio

-Oss

mix

ed

wit

hau

tog

en

ou

sb

on

e

Pati

en

tMate

rial

an

dm

eth

od

sLe

ng

tho

fo

bse

rvati

on

peri

od

Ou

tco

me

measu

res

Refe

ren

ce

Pri

mary

Seco

nd

ary

10

12

sin

use

sw

ith

50%

Bio

-Oss

an

d50%

ilia

cb

on

e30

Fria

lit-

2im

pla

nts

30

bio

psi

es

aft

er

6m

on

ths

6m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

100%

5m

on

ths

7m

on

ths

PC

:N

on

eM

aio

ran

aet

al.

(2000)

Bio

-Oss

em

bed

ded

infi

bro

us

tiss

ue

Lim

ited

bo

ne

reg

en

era

tio

n

Bio

-Oss

surr

ou

nd

ed

an

din

terc

on

nect

ed

by

new

lyb

on

e

20

30

sin

use

sw

ith

80%

Bio

-Oss

an

d20%

chin

bo

ne

79

Bra

nem

ark

imp

lan

tsaft

er

6m

on

ths

16

an

d12

bio

psi

es

aft

er

6m

on

ths

an

d3

years

,re

spect

ively

6m

on

ths

to3

year

Sup

rast

ruct

ure

:N

RIm

pla

nt:

90%

Co

nn

ect

ive

tiss

ue

6m

on

ths

3ye

ar

PC

:N

RH

all

man

et

al.

(2001a,

2001b

)54%

36%

Lam

ell

ar

bo

ne

21%

51%

Imm

atu

reb

on

e10%

1%

Resi

du

al

Bio

-Oss

15%

12%

12

13

sin

use

sw

ith

Bio

-Oss

an

da

mix

ture

of

bo

ne

fro

mch

in,

retr

om

ola

rare

ao

rtu

bero

sity

36

Bra

nem

ark

imp

lan

tsaft

er

7m

on

ths

23

bio

psi

es

aft

er

7m

on

ths

6–9

.5m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

100%

NFB

Co

nn

ect

ive

tiss

ue

Resi

du

al

Bio

-Oss

PC

:N

ose

ble

ed

ing

:17%

Deh

isce

nce

:8%

Yil

dir

imet

al.

(2001)

19%

52%

30%

20

30

sin

use

sw

ith

80%

Bio

-Oss

an

d20%

chin

bo

ne

79

Bra

nem

ark

imp

lan

taft

er

6m

on

ths

3m

on

ths

to2

year

Sup

rast

ruct

ure

:N

RIm

pla

nt:

92%

Heig

ht

of

gra

ft:

PC

:In

fect

ion

wit

hB

io-O

ssexf

oli

ate

d:

10%

Hall

man

et

al.

(2002b

)3

mo

nth

s12

mo

nth

s24

mo

nth

s16

mm

15

mm

14.5

mm

20

30

sin

use

sw

ith

80%

Bio

-Oss

an

d20%

chin

bo

ne

79

Bra

nem

ark

imp

lan

tsaft

er

6m

on

ths

5ye

ars

Sup

rast

ruct

ure

:95%

Imp

lan

t:89%

NR

PC

:In

fect

ion

wit

hB

io-O

ssexf

oli

ate

d:

10%

Mu

cosa

lsi

nu

sch

an

ges:

29%

Hall

man

&Zett

erq

vist

(2004)

191

294

sin

use

sw

ith

33%

Bio

-Oss

an

d66%

chin

or

ram

us

bo

ne

426

Bra

nem

ark

imp

lan

tsaft

er

6–9

mo

nth

s

0–6

mo

nth

s7–1

2m

on

ths

13–2

4m

on

ths

97–1

08

mo

nth

s

Sup

rast

ruct

ure

:N

RIm

pla

nt:

94%

Gra

fted

heig

ht/

ori

gin

al

heig

ht

rati

o:

3.5

32.2

1.9

30.7

9

PC

:N

RH

ata

no

et

al.

(2004)

811

sin

use

sw

ith

30%

Bio

-Oss

an

d70%

ram

us

or

ilia

cb

on

e32

Fria

lit-

2o

rB

ran

em

ark

imp

lan

tssi

mu

ltan

eo

usl

y

5ye

ars

Sup

rast

ruct

ure

:N

RIm

pla

nt:

88%

NR

PC

:In

fect

ion

:3%

Wo

un

dd

eh

isce

nce

:10%

Marc

hett

iet

al.

(2007)

22

37

sin

use

sw

ith

30%

Bio

-Oss

an

d70%

ram

us

or

ilia

cb

on

e108

Fria

lit-

2o

rB

ran

em

ark

imp

lan

tsaft

er

5m

on

ths

Sup

rast

ruct

ure

:N

RIm

pla

nt:

97%

20

20

sin

use

sw

ith

50%

Bio

-Oss

an

d50%

bo

ne

fro

mtu

bero

sity

44

Zim

mer

imp

lan

tssi

mu

ltan

eo

usl

y

1ye

ar

Sup

rast

ruct

ure

:N

RIm

pla

nt:

89%

NR

PC

:Se

vere

acu

tesi

nu

siti

s:5%

Ab

scess

:5%

Can

niz

zaro

et

al.

(2009)

10

15

sin

use

sw

ith

Bio

-Oss

an

dsm

all

volu

mes

of

bo

ne

fro

mtu

bero

sity

an

dlo

cal

bo

ne

30

Oss

tem

imp

lan

tssi

mu

ltan

eo

usl

y

1ye

ar

Sup

rast

ruct

ure

:100%

Imp

lan

t:98%

Alv

eo

lar

bo

ne

heig

ht

PC

:Si

nu

siti

s:7

.5%

Wo

un

dd

eh

isce

nce

Nasa

lb

leed

ing

Infe

ctio

ns,

swell

ing

Sen

sory

pro

ble

ms

of

up

per

lip

Kim

et

al.

(2009)

Befo

resu

rgery

Aft

er

surg

ery

1ye

ar

5.1

mm

19

mm

16.9

mm

68

sin

use

sw

ith

Bio

-Oss

an

dsm

all

volu

mes

of

bo

ne

fro

mtu

bero

sity

an

dlo

cal

bo

ne

19

Oss

tem

imp

lan

tsaft

er

4–7

mo

nth

s

4.7

mm

19.2

mm

17.7

mm



Galindo-Moreno et al. 2010a, 2010b), and the

proportion of newly formed bone seemed to

increase with the length of the observation period

(Hallman et al. 2001a).

Summary. Bio-Oss and Bio-Oss mixed with

autogenous bone seem to induce comparable

proportions of new bone formation. However,

the graft in the comparative studies consisted

mainly of Bio-Oss.

BIC and biomechanical test values, experimental im-plants

Comparative studies. BIC was assessed after place-

ment of an experimental microimplant 6–9

months after MSFA with Bio-Oss or with a mix-

ture of 80% Bio-Oss and 20% autogenous man-

dibular bone (Hallman et al. 2002a). No

statistically significant difference in BIC was re-

ported when Bio-Oss was used (32%) as compared

with mixed Bio-Oss and autogenous bone (54%)

after 6 months.

Supplementary studies. A BIC of 55% has been

reported 8 months after simultaneous placement

of experimental implants in sinuses augmented

with Bio-Oss (Lindgren et al. 2009).

Summary. The two treatment modalities seem

to induce comparable BIC. However, the mixed

graft consisted mainly of Bio-Oss. Biomechanical

implant test values have never been compared.

Biodegradation of Bio-Oss

Comparative studies. No biodegradation of Bio-

Oss particles was reported 13–15 months after

MSFA with Bio-Oss or with a mixture of 80%

Bio-Oss and 20% autogenous mandibular bone

(Hallman et al. 2002a).

Supplementary studies. In most studies, no or

limited biodegradation was identified 6–48

months after MSFA with Bio-Oss (Piattelli et

al. 1999; Yildirim et al. 2000; Orsini et al. 2005;

Degidi et al. 2006; Lee et al. 2006; Ferreira et al.

2009). However, extensive biodegradation was

reported after 12–13 months in two studies

(Valentini et al. 2000; Fugazzotto 2003). More-

over, complete Bio-Oss biodegradation was seen

after 12–13 months (Fugazzotto 2003).

No biodegradation of Bio-Oss was identified

up to 36 months after MSFA with Bio-Oss mixed

with autogenous bone (Maiorana et al. 2000;

Hallman et al. 2001a; Yildirim et al. 2001; de

Vicente et al. 2010).

Summary. Most studies indicate that Bio-Oss

undergoes no or limited biodegradation. Addition

of autogenous bone to Bio-Oss seems not to

influence the biodegradation of Bio-Oss. How-

ever, long-term studies are not available.

Volumetric stability of the graft

Comparative studies. No study was identified.

Supplementary studies. The volumetric stability

of the graft after MSFA with Bio-Oss has never

been assessed.

The volumetric stability of Bio-Oss mixed

with autogenous bone has been evaluated by

two-dimensional quantitative methods (Hallman

et al. 2002b; Hatano et al. 2004; Kim et al. 2009;

Galindo-Moreno et al. 2010a). When 80% Bio-

Oss and 20% autogenous mandibular bone was

used, o10% of the originally augmented region

was resorbed after 24 months (Hallman et al.

2002b). After application of a mixture of 33%

Bio-Oss and 66% autogenous mandibular bone,

the upper part of the graft was located above the

implants immediately after the augmentation

procedure, whereas the grafted sinus floor was

located at the implant tip level or slightly below

after 2–3 years (Hatano et al. 2004). Height

reduction of the originally augmented region

was 1.8 mm after 1 year when Bio-Oss was

mixed with a small volume of autogenous max-

illary bone (Kim et al. 2009), and diminished

height reduction of the augmented region was

observed with a higher proportion of remaining

Bio-Oss particles in the graft after 6 months

(Galindo-Moreno et al. 2010a).

Summary. The volumetric stability of the graft

after MSFA with the two treatment modalities

has never been compared within the same study.

Postoperative complications, augmented region

Comparative studies. One study reported no

postoperative complications (John & Wenz

2004).

Supplementary studies. MSFA with Bio-Oss

showed no postoperative complications in five

studies (Tawil & Mawla 2001; Artzi et al. 2002;

Mangano et al. 2007; Lindgren et al. 2009;

Lambert et al. 2010). Postoperative infection

occurred rarely (Valentini & Abensur 2003; Hall-

man & Nordin 2004; Mardinger et al. 2007;

Ferreira et al. 2009), and total removal of the

graft was necessary in 0.5% of the cases due to

persistent infection (Ferreira et al. 2009). Partial

graft failure due to infection occurred in 5%,

requiring an additional augmentation procedure

at the time of implant placement (Valentini et al.

2000). Nose bleeding was reported in 20% and

33% of the cases, respectively, in two studies

(Yildirim et al. 2000; Lee et al. 2006).

34

10

sin

use

sw

ith

Bio

-Oss

an

db

on

efr

om

maxi

lla

No

.o

fim

pla

nts

sim

ult

an

eo

usl

y:N

R9

mo

nth

sto

34

mo

nth

sSu

pra

stru

ctu

re:

NR

Imp

lan

t:99%

NFB

Co

nn

ect

ive

tiss

ue

Resi

du

al

Bio

-Oss

PC

:In

fect

ion

:5%

de

Vic

en

teet

al.

(2010)

32

sin

use

sw

ith

Bio

-Oss

an

db

on

efr

om

maxi

lla

No

.o

fim

pla

nts

aft

er

9m

on

ths:

NR

14

bio

psi

es

aft

er

9m

on

ths

29%

21%

50%

45

90

sin

use

sw

ith

50%

Bio

-Oss

an

d50%

bo

ne

fro

mm

axi

lla

52

Mic

rod

en

tan

d38

Ast

raim

pla

nts

aft

er

6m

on

ths

90

bio

psi

es

aft

er

6m

on

ths

2ye

ar

Sup

rast

ruct

ure

:N

RIm

pla

nt:

NR

NFB

:46%

Rad

iog

rap

hic

gra

ftre

du

ctio

n:

PC

:N

RG

ali

nd

o-

Mo

ren

oet

al.

(2010a)

Co

nn

ect

ive

tiss

ue:

42%

o30%

resi

du

al

Bio

-O

ssin

gra

ft0.4

mm

Resi

du

al

Bio

-Oss

:37%

430%

resi

du

al

Bio

-O

ssin

gra

ft0.2

mm

25

45

sin

use

sw

ith

50%

Bio

-Oss

an

d50%

bo

ne

fro

mm

axi

lla

26

Mic

rod

en

tan

d19

Ast

raim

pla

nts

aft

er

6m

on

ths

45

bio

psi

es

aft

er

6m

on

ths

2ye

ar

Sup

rast

ruct

ure

:N

RIm

pla

nt:

100%

NFB

Co

nn

ect

ive

tiss

ue

Resi

du

al

Bio

-Oss

PC

:N

on

eG

ali

nd

o-

Mo

ren

oet

al.

(2010b

)35%

32%

33%

All

gro

up

valu

es

refe

rred

toare

exp

ress

ed

as

mean

valu

es.

NFB

,n

ew

lyfo

rmed

bo

ne;

NR

,n

ot

rep

ort

ed

;PC

,p

ost

op

era

tive

com

plica

tio

ns.



In two studies, no postoperative complications

were reported with mixed Bio-Oss and autoge-

nous bone (Maiorana et al. 2000; Galindo-Mor-

eno et al. 2010b). Removal of inserted implants

due to severe acute sinusitis and abscess has been

reported in one study with mixed Bio-Oss and

autogenous bone (Cannizzaro et al. 2009). Infec-

tion with exfoliation of Bio-Oss particles has

been reported in 10% (Hallman et al. 2002b;

Hallman & Zetterqvist 2004), while infection,

wound dehiscence, swelling, hematoma, nose

bleeding, and sensory disturbances of the upper

lip were reported infrequently (Yildirim et al.

2001; Marchetti et al. 2007; Kim et al. 2009; de

Vicente et al. 2010). CT scans obtained 3 years

after MSFA showed that 29% of the augmented

sinuses had asymptomatic changes of the max-

illary sinus mucosa (Hallman & Zetterqvist

2004). No serious postoperative complications

including disease transmission were reported in

any of the studies.

Summary. The frequency and severity of post-

operative complications with the two treatment

modalities seem to be comparable. However, the

occurrence of complications has never been com-

pared within the same study.

Discussion

The current knowledge about implant treatment

involving MSFA with Bio-Oss or Bio-Oss mixed

with autogenous bone as graft was assessed in the

present systematic review to test the hypothesis

of no differences between the two treatment

modalities. A total of 35 studies using the lateral

window technique were included (Piattelli et al.

1999; Maiorana et al. 2000; Valentini et al. 2000;

Yildirim et al. 2000; Hallman et al. 2001a,

2001b; Tawil & Mawla 2001; Yildirim et al.

2001; Artzi et al. 2002; Hallman et al. 2002a,

2002b; Fugazzotto 2003; Valentini & Abensur

2003; Hallman & Nordin 2004; Hallman &

Zetterqvist 2004; Hatano et al. 2004; John &

Wenz 2004; Orsini et al. 2005; Degidi et al. 2006;

Froum et al. 2006; Lee et al. 2006; Mangano et al.

2007; Marchetti et al. 2007; Mardinger et al.

2007; Cordaro et al. 2008; Froum et al. 2008;

Simunek et al. 2008; Cannizzaro et al. 2009;

Ferreira et al. 2009; Kim et al. 2009; Lindgren et

al. 2009; de Vicente et al. 2010; Galindo-Moreno

et al. 2010a, 2010b; Lambert et al. 2010). No

long-term study comparing MSFA with the two

treatment modalities was identified.

The primary outcome measures are the most

important measures for the assessment of the

treatment outcome. However, secondary outcome

measures were also included in the present sys-

tematic review as surrogate measures due to the

frequent lack of studies focusing on primary out-

come measures. In addition, supplementary stu-

dies involving MSFA with either Bio-Oss or Bio-

Oss mixed with autogenous bone were included.

The survival of the suprastructures after MSFA

with Bio-Oss or Bio-Oss mixed with autogenous

bone has never been compared within the same

study. Implant survival using Bio-Oss or Bio-Oss

mixed with autogenous bone has exclusively

been compared in one study and no statistically

significant differences were revealed (Hallman

et al. 2002a). The 1-year implant survival was

Table 4. Quality assessment

Adequate randomization ofBio-Oss and Bio-Ossmixed with autogenous bone

Blinding of outcomeassessment

Completenessof follow-up

Histologic evaluationinvolving unbiasedstereologic methods

Risk of Bias Reference

– No – No High Piattelli et al. (1999)– No – No High Maiorana et al. (2000)– No – No High Valentini et al. (2000)– No – No High Yildirim et al. (2000)– No – No High Hallman et al. (2001a)– No – No High Hallman et al. (2001b)# No Yes – High Tawil & Mawla (2001)– No – No High Yildirim et al. (2001)– No – No High Artzi et al. (2002)No No Yes No High Hallman et al. (2002a)– No Yes No High Hallman et al. (2002b)– No – No High Fugazzotto (2003)– No – – High Valentini & Abensur (2003)– No – – High Hallman & Nordin (2004)– No No – High Hallman & Zetterqvist (2004)– No – No High Hatano et al. (2004)No No – No High John & Wenz (2004)– No – No High Orsini et al. (2005)– No – No High Degidi et al. (2006)# # No No High Froum et al. (2006)– No – No High Lee et al. (2006)– No Yes No High Mangano et al. (2007)– No – – High Marchetti et al. (2007)– No – - High Mardinger et al. (2007)# No No No High Cordaro et al. (2008)# # No No High Froum et al. (2008)No No Yes No High Simunek et al. (2008)– No – No High Ferreira et al. (2009)# Yes Yes – High Cannizzaro et al. (2009)– No – – High Kim et al. (2009)# No Yes No High Lindgren et al. (2009)– No – No High De Vicente et al. (2010)– No Yes No High Galindo-Moreno et al. (2010a)– No Yes No High Galindo-Moreno et al. (2010b)– No No – High Lambert et al. (2010)

–, not relevant; #, randomization and blinding of outcome assessment performed for other treatment modalities.



96% with Bio-Oss and 94% with a mixture of

80% Bio-Oss and 20% autogenous mandibular

bone. The survival of suprastructures and im-

plants after MSFA with autogenous bone has

been evaluated in several studies, including

long-term studies, as reported in several reviews

(Tong et al. 1998; Wallace & Froum 2003; Del

Fabbro et al. 2004; Esposito et al. 2006; Pjeturs-

son et al. 2008; Chiapasco et al. 2009; Jensen &

Terheyden 2009; Nkenke & Stelzle 2009). The

survival of the suprastructures and the implants

within the short-term studies of the present

systematic review seems to be similar to the

outcome obtained with autogenous bone grafts.

Histologic evaluation of biopsies after MSFA

with the two treatment modalities revealed that

the Bio-Oss particles were incorporated in newly

formed bone, and the proportion of newly formed

bone appeared to increase with the length of the

observation period (Piattelli et al. 1999; Hallman

et al. 2001a). No statistically significant differ-

ence in bone regeneration was revealed with Bio-

Oss or Bio-Oss mixed with autogenous bone

(Hallman et al. 2002a; John & Wenz 2004;

Simunek et al. 2008). However, the graft con-

sisted mainly of Bio-Oss with a limited amount

of autogenous bone. Moreover, the mean healing

period was 6.5 months for Bio-Oss mixed with

autogenous bone, while the corresponding heal-

ing period for Bio-Oss was 8.5 months (Hallman

et al. 2002a). The above-mentioned results may

be compromised by the use of biased histomor-

phometry (Gundersen et al. 1988a, 1988b).

A recently published review assessing the total

bone volume after MSFA based on histomorpho-

metric analysis demonstrated a statistically sig-

nificantly higher proportion of mineralized bone

during the early healing phase when autogenous

bone is used as graft as compared with various

bone substitutes used alone or in combination

with autogenous bone (Handschel et al. 2009). It

may therefore be hypothesized that a higher

proportion of autogenous bone than the pre-

viously evaluated 10–33% may accelerate new

bone formation when Bio-Oss mixed with auto-

genous bone is used as graft. However, healing

periods of more than 9 months revealed no

statistically significant differences between the

treatment modalities (Handschel et al. 2009).

Therefore, accelerated bone formation within

the initial healing period may be possible by

increasing the proportion of autogenous bone

when mixed Bio-Oss and autogenous bone is

used as graft.

No statistically significant difference was re-

ported in BIC when Bio-Oss, a mixture of 80%

Bio-Oss and 20% autogenous bone, and autoge-

nous bone was used as graft (Hallman et al.

2002a). However, further studies are needed to

assess whether a higher proportion of autogenous

bone in the mixed graft may enhance BIC com-

pared with Bio-Oss.

Most studies indicate that Bio-Oss undergoes

no or limited biodegradation (Piattelli et al. 1999;

Yildirim et al. 2000; Orsini et al. 2005; Degidi et

al. 2006; Lee et al. 2006). Addition of autogenous

bone to Bio-Oss does not seem to influence the

biodegradation of Bio-Oss (Maiorana et al. 2000;

Hallman et al. 2001a; Yildirim et al. 2001; de

Vicente et al. 2010). However, long-term studies

evaluating the biodegradation of Bio-Oss are

lacking, but case reports have demonstrated the

presence of Bio-Oss particles 9–10 years after

MSFA with Bio-Oss (Sartori et al. 2003; Traini

et al. 2007).

The volumetric stability of the graft after

MSFA with Bio-Oss or Bio-Oss mixed with

autogenous bone has never been compared. Lim-

ited volumetric changes of the graft seem to occur

with different mixtures of Bio-Oss and autoge-

nous bone (Hallman et al. 2002b; Hatano et al.

2004; Kim et al. 2009; Galindo-Moreno et al.

2010a). However, these results may be compro-

mised by the use of two-dimensional quantitative

methods involving calliper on radiographs.

Therefore, further studies using three-dimen-

sional quantification are needed to assess

whether Bio-Oss or Bio-Oss mixed with auto-

genous bone may be beneficial for graft preserva-

tion. Also, studies focusing upon the influence of

different ratios of Bio-Oss and autogenous bone

on the volumetric stability of the graft are needed.

MSFA with autogenous bone alone is character-

ized by unpredictable graft resorption (Johansson

et al. 2001; Wiltfang et al. 2005; Zizelmann et al.

2007). Therefore, it may be hypothesized that

addition of Bio-Oss to the autogenous bone graft

may be an advantage for the preservation of the

initially augmented graft volume due to the

apparently sparse or limited biodegradation of

Bio-Oss.

Postoperative complications related to the aug-

mented region were not reported in all studies,

but when reported, they were generally low and

not severe. The frequency of postoperative com-

plications with the two treatment modalities

seems to be in accordance with the frequency of

complications after using autogenous bone, as

reported previously in systematic reviews (Pje-

tursson et al. 2008; Chiapasco et al. 2009;

Nkenke & Stelzle 2009). Assessment of post-

operative complications after MSFA should also

include donor site morbidity after autogenous

bone harvesting. However, this aspect has exclu-

sively been addressed in three of the included

studies (Hallman et al. 2002b; Hallman & Zet-

terqvist 2004; Marchetti et al. 2007).

Conclusions

The hypothesis of no differences between Bio-

Oss or Bio-Oss mixed with autogenous bone as

graft for MSFA applying the lateral window

technique could neither be confirmed nor re-

jected due insufficient knowledge. Long-term

clinical and radiographic studies focusing on im-

plant treatment involving MSFA with Bio-Oss or

Bio-Oss mixed with autogenous bone are needed

before final conclusions can be made.

Potential conflict of interest: Thomas Jensen

has received biomaterials from Geistlich Pharma

for a PhD study evaluating a mixture of Bio-Oss

and autogenous bone in different ratios for MSFA

in minipigs.

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